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MEMCAL    SCHOOL 
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THE  EARLY  EMBRYOLOGY 

OF 

THE   CHICK 


PATTEN 


THE  EARLY  EMBRYOLOGY 

OF 

THE    CHICK 


BY 


BRADLEY  M.  PATTEN 

ASSISTANT  PROFESSOR  OF  HISTOLOGY  AND  EMBRYOLOGY 
SCHOOL    OF    MEDICINE,    WESTERN    RESERVE    UNIVERSITY 


WITH   55   ILLUSTRATIONS  CONTAINING 
182  FIGURES 


PHILADELPHIA 

P.  BLAKISTON'S  SON  &  CO 

1012  WALNUT  STREET 


Copyright,  1920,  by  P.  Blakiston's  Son  &  Co. 


•  •    •  • 

•  •  •        • 


•  •  •  •  •  • 

•  ••••»    ; 

«    •  •  •  •  •    • 

,     • 


'   -♦.    .», 


.••  •  ••:     : 


TKK     M^I>X.K     X>HKBS     YOKKL    PA 


151 


PREFACE 

The  fact  that  most  courses  in  vertebrate  embryology  deal  to 
a  greater  or  lesser  extent  with  the  chick  seems  to  warrant  the 
treatment  of  its  development  in  a  book  designed  primarily 
for  the  beginning  student.  To  a  student  beginning  the  study 
of  embryology  the  very  abundance  of  information  available  in 
the  literature  of  the  subject  is  confusing  and  discouraging.  He 
is  unable  to  cull  the  essentials  and  fit  them  together  in  their 
proper  relationships  and  is  Hkely  to  become  hopelessly  lost  in  a 
maze  of  details.  This  book  was  written  in  an  effort  to  set  forth 
for  him  in  brief  and  simple  form  the  early  embryology  of  the 
chick.  It  does  not  purport  to  treat  the  subject  from  the  com- 
parative view  point,  nor  to  be  a  reference  work.  If  it  helps  the 
student  to  grasp  the  structure  of  the  embryos,  and  the  sequence 
and  significance  of  the  processes  he  encounters  in  his  work  on  the 
chick,  and  thereby  conserves  the  time  of  the  instructor  for  inter- 
pretation of  the  broader  principles  of  embryology  it  will  have 
served  the  purpose  for  which  it  was  written. 

In  preparing  the  text,  details  have  been  largely  omitted  and 
controverted  points  avoided  for  the  sake  of  clarity  in  outHning 
fundamental  processes.  While  I  would  gladly  have  avoided 
the  matters  of  cleavage  and  germ  layer  formation  in  birds,  a 
brief  description  of  them  seemed  necessary.  Without  some 
interpretation  of  the  initial  phases  of  development,  the  student 
has  no  logical  basis  for  his  study  of  the  already  considerably 
developed  embryos  with  which  his  laboratory  work  begins. 
The  treatment  which  it  is  desirable  to  accord  to  gametogenesis 
and  maturation  as  processes  leading  toward  fertilization  would 
vary  so  greatly  in  extent  and  view  point  in  different  courses 
that  it  seemed  inadvisable  to  attempt  any  general  discussion 
of  these  phenomena. 

The  account  of  development  has  not  been  carried  beyond  the 
first  four  days  of  incubation.  In  this  period  the  body  of  the 
embryo  is  laid  down  and  the  organ  systems  are  estabHshed. 
Courses  in  general  embryology  rarely  carry  work  on  the  chick 
beyond  this  phase  of  development.     More  extensive  courses  in 

V 


VI  PREFACE 

which  a  knowledge  of  mammalian  embryology  is  the  objective, 
ordinarily  pass  from  the  study  of  three  or  four  day  chicks  to 
work  on  mammalian  embryos. 

While  the  text  has  been  kept  brief,  illustrations  have  been 
freely  used  in  the  belief  that  they  convey  ideas  more  readily 
and  more  accurately  than  can  be  done  in  writing.  Direct 
labeling  has  been  used  in  the  figures  to  facilitate  reference  to 
them.  Most  of  the  drawings  were  made  directly  from  prepara- 
tions in  the  laboratory  of  Histology  and  Embryology  of  Western 
Reserve  University  School  of  Medicine.  However,  figures  from 
other  authors,  particularly  Lillie  and  Duval,  have  been  used 
extensively  for  comparisons  and  for  schemes  of  presentation. 
Several  figures  have  been  reproduced  directly  or  with  only 
slight  modifications.  These  are  designated  in  the  figure 
legends. 

I  wish  to  acknowledge  the  assistance  I  received  in  the  prepa- 
ration of  material  by  Mrs.  Mary  V.  Bayes,  and  in  the  drawing 
of  the  figures  by  Mrs.  Bayes  and  Dr.  Louis  J.  Karnosh.  I  am 
also  indebted  to  my  father.  Prof.  Wm.  Patten  of  Dartmouth 
College  for  criticism  of  the  figures,  and  to  Dr.  F.  C.  Waite  of  the 
School  of  Medicine,  Western  Reserve  University  for  his  helpful 
interest  and  cooperation  in  all  phases  of  the  preparation  of  the 
book  and  especially  for  his  reading  of  the  manuscript. 

Beadley  M.  Patten. 
Western  Reserve  University, 
School  of  Medicine. 
Cleveland,  Ohio. 


CONTENTS 


Page 
Preface v 

CHAPTER  I 
Introduction i 

CHAPTER  II 

The  Gametes  and  Fertilization 7 

The  ovarian  ovum;  maturation,  ovulation,  and  fertilization;  the 
formation  of  the  accessory  coverings  of  the  ovum;  the  structure  of 
the  egg  at  the  time  of  laying;  incubation. 

CHAPTER  III 

The  Process  of  Segmentation 14 

The  effect  of  yolk  on  segmentation;  the  unsegmented  blastodisc;  the 
sequence  and  orientation  of  the  cleavage  di\dsions  in  birds. 

CHAPTER  IV 

The  Establishment  of  the  Entoderm 20 

The  morula  stage;  the  formation  of  the  bias  tula;  the  effect  of  yolk  on 
gastrulation;  gastrulation  in  birds. 

CHAPTER  V 

The  Formation  of  the  Primitive  Streak  and  the  Establishment  of 

THE  Mesoderm 27 

The  location  and  appearance  of  the  primitive  streak;  the  origin  of  the 
primitive  streak  by  concrescence  of  the  blastopore;  the  formation  of 
the  mesoderm. 

CHAPTER  VI 

From  the  Primitive  Streak  Stage  to  the  Appearance  of  the  Somites      ss 
The  primitive  streak  as  a  center  of  growth;  the  growth  of  the  entoderm 
and  the  establishment  of  the  primitive  gut;  the  growth  and  differ- 
entiation of  the  mesoderm;  the  formation  of  the  notochord;  the  forma- 
tion of  the  neural  plate;  the  differentiation  of  the  embryonal  area. 

CHAPTER  VII 

The  Structure  OF  Twenty-four  Hour  CmCKS 44 

The  formation  of  the  head;  the  formation  of  the  neural  groove;  the 
regional  divisions  of  the  mesoderm;  the  coelom;  the  pericardial  region; 
the  area  vasculosa. 


Vlll  CONTENTS 

CHAPTER  VIIl 

Page 
The  Changes  Between   Twenty-four  and  Thirty-three  Hours  of 

Incubation 52 

The  closure  of  the  neural  tube;  the  diflferentiation  of  the  brain  region; 
the  anterior  neuropore;  the  sinus  rhomboidalis;  the  fate  of  the  primitive 
streak;  the  formation  of  additional  somites;  the  lengthening  of  the 
fore-gut;  the  appearance  of  the  heart  and  the  omphalomesenteric 
veins;  organization  in  the  area  vasculosa. 

CHAPTER  IX 

The  Structure  op  Chicks  Between  Thirty-three  and  Thirty-nine 

Hours  of  Incubation 59 

The  divisions  of  the  brain  and  their  neuromeric  structure;  the  auditory 
pits;  the  formation  of  extra-embryonic  blood  vessels;  the  formation  of 
the  heart;  the  formation  of  intra-embryonic  blood  vessels. 

CHAPTER  X 

The  Changes  Between  Forty  and  Fifty  Hours  of  Incubation 75 

Flexion  and  torsion;  the  completion  of  the  vitelline  circulatory  channels; 
the  beginning  of  the  circulation  of  blood. 

CHAPTER  XI 

Extra-embryonic  Membranes 80 

The  folding  of!  of  the  body  of  the  embryo;  the  establishment  of  the 
yolk-sac  and  the  delimitation  of  the  embryonic  gut;  the  amnion  and  the 
serosa;  the  allantois. 

CHAPTER  XII 

The  Structure  of  Chicks  from   Fifty  to  Fifty-five   Hours  of  In- 
cubation   93 

I.  External  Features. 
II.  The  Nervous  System. 

Growth  of  the  telencephalic  region;   the  epiphysis;   the  in- 
fundibulum  and  Rathke's  pocket;  the  optic  vesicles;  the  lens; 
the  posterior  part  of  the  brain  and  the  cord  region  of  the  neural 
tube;  the  neural  crests. 
HI.  The  Digestive  Tract. 

The  fore-gut;  the  stomodaeum;  the  pre-oral  gut;  the  mid-gut; 
the  hind-gut. 
IV.  The  Visceral  Clefts  and  Visceral  Arches. 
V.  The  Circulatory  System. 

The  heart;  the  aortic  arches;  the  fusion  of  the  dorsal  aortse;  the 
cardinal  and  omphalomesenteric  vessels. 
VI.  The  Differentiation  of  the  Somites. 
Vn.  The  Urinary  System. 


CONTENTS 


IX 


CHAPTER  XIII 


Page 


The  Development  of  the  Chick  During  the  Third  and  Fourth  Days 

OF  Incubation 109 

I.  External  Features. 

Torsion;  flexion;  the  visceral  arches  and  clefts;  the  oral  region; 
the  appendage  buds;  the  allantois. 
II.  The  Nervous  System. 

Summary  of  development  prior  to  the  third  day;  the  formation 
of  the  telencephalic  vesicles;  the  diencephalon;  the  mesen- 
cephalon; the  metencephalon;  the  myelencephalon;  the  ganglia 
of  the  cranial  nerves;  the  spinal  cord;  the  spinal  nerve  roots. 

III.  The  Sense  Organs. 

The  eye;  the  ear;  the  olfactory  organs. 

IV.  The  Digestive  and  Respiratory  Systems. 

Summary  of  development  prior  to  the  third  day;  the  establish- 
ment of  the  oral  opening;  the  pharyngeal  derivatives;  the 
trachea;  the  lung-buds;  the  oesophagus  and  stomach;  the 
liver;  the  pancreas;  the  mid-gut  region;  the  cloaca;  the  procto- 
daeum  and  the  cloacal  membrane. 
V.  The  Circulatory  System. 

The  functional  significance  of  the  embryonic  circulation;  the 
vitelline  circulation;  the  allantoic  circulation;  the  intra-embry- 
onic  circulation;  the  heart. 
VI.  The  Urinary  System. 

The  general  relationships  of  pronephros,  mesonephros,  and 
metanephros;  the  pronephric  tubules  of  the  chick;  the  meso- 
nephric  tubules. 
VII.  The  Coelom  and  Mesenteries. 


APPENDIX 

References  for  Collateral  Reading 155 

Index 161 


CHAPTER  I 


INTRODUCTION 


The  only  method  of  attaining  a  comprehensive  understanding 
of  embryological  processes  is  through  the  study  and  comparison 
of  development  in  various  animals.  Many  phases  of  the 
development  of  any  specific  organism  can  be  interpreted  only 
through  a  knowledge  of  corresponding  processes  in  other 
organisms.  The  beginning  student,  however,  must  acquire  his 
knowledge  of  embryology  through  intensive  study  of  one  form 
at  a  time,  depending  at  first  on  older  workers  in  the  field  for 
interpretation  of  the  phenomena  encountered.  Building  on 
the  f amiharity  with  fundamental  processes  of  development  thus 
acquired,  he  may  later  broaden  his  horizon  by  the  comparative 
study  of  a  variety  of  forms. 

The  chick  is  one  of  the  most  satisfactory  animals  on  which 
student  laboratory  work  in  embryology  may  be  based.  Chick 
embryos  in  a  proper  state  of  preservation  and  of  the  stages 
desired  can  be  readily  secured  and  prepared  for  study.  Used 
as  the  only  laboratory  material  in  a  brief  course  they  afford  a 
basis  for  understanding  the  early  differentiation  of  the  organ 
systems  and  the  fundamental  processes  of  body  formation 
common  to  all  groups  of  vertebrates.  In  more  extended  courses 
where  several  forms  are  taken  up,  the  chick  serves  at  once  as  a 
type  for  the  development  characteristic  of  the  large-yolked 
eggs  of  birds  and  reptiles,  and  as  an  intermediate  form  bridging 
the  gap  between  the  simpler  processes  of  development  in  fishes 
and  amphibia  on  the  one  hand  and  the  more  complex  processes 
in  mammals  on  the  other.  In  medical  school  courses  where  a 
knowledge  of  human  embryology  is  the  end  in  view  the  chick 
not  only  makes  a  good  stepping  stone  to  the  understanding  of 
mammalian  embryology,  but  also  provides  material  for  the 
study  of  early  developmental  processes  not  readily  demon- 
strable in  mammalian  material. 

This  book  on  the  development  of  the  chick  has  been  written 


2  EARLY   EMBRYOLOGY    OF    THE    CHICK 

for  those  who  are  beginning  the  study  of  embryology  and  has 
accordingly  been  kept  as  brief  and  as  uncomplicated  as  possible. 
Nevertheless  it  is  assumed  that  the  beginner  in  embryology 
will  not  be  without  a  certain  back-ground  of  zoological 
knowledge  and  training.  He  may  reasonably  be  expected  to 
be  familiar  with  some  of  the  aspects  of  evolution  and  heredity, 
with  the  recapitulation  theory,  the  cell  theory,  the  nature  of 
the  various  types  of  tissues,  and  the  more  general  phases  of 
the  morphology  of  vertebrates.  Before  laboratory  work  on 
the  chick  is  begun  in  any  course  in  embryology  the  nature  of 
sexual  reproduction,  and  the  processes  of  gametogenesis, 
maturation,  fertilization  and  cleavage,  will  have  been  taken 
up.  It  therefore  seems  unnecessary  to  include  here  any  pre- 
liminary, general  discussion  of  these  phenomena.  References 
for  collateral  reading  on  this  and  other  phases  of  the  subject 
are  given  in  the  appendix. 

Like  other  sciences  embryology  demands  first  of  all  accurate 
observation.  It  differs  considerably,  however,  from  such  a 
science  as  adult  anatomy  where  the  objects  studied  are  rela- 
tively constant  and  their  component  parts  are  not  subject  to 
rapid  changes  in  their  inter-relations.  During  development, 
structural  conditions  within  the  embryo  are  constantly  chang- 
ing. Each  phase  of  development  presents  a  new  complex  of 
conditions  and  new  problems. 

Solution  of  the  problems  presented  in  any  given  stage  of 
development  depends  upon  a  knowledge  of  the  stages  which 
precede  it.  To  comprehend  the  embryology  of  an  organism 
one  must,  therefore,  start  at  the  beginning  of  its  development 
and  follow  in  their  natural  order  the  changes  which  occur. 
At  the  outset  of  his  work  the  student  must  realize  that  proper 
sequence  of  study  is  essential  and  may  not  be  disregard-ed.  A 
knowledge  of  structural  conditions  in  earlier  stages  than  that 
at  the  moment  under  consideration,  and  an  appreciation  of  the 
trend  of  the  developmental  processes  by  which  conditions  at 
one  stage  become  transmuted  into  different  conditions  in  the 
next,  are  direct  and  necessary  factors  in  acquiring  a  real  com- 
prehension of  the  subject.  Without  them  the  story  of 
embryology  becomes  incoherent,  a  mere  jumble  of  confused 
impressions. 

A  knowledge  of  the  phenomena  of  development  is  ordinarily 


INTRODUCTION  3 

acquired  by  studying  a  series  of  embryos  at  various  stages  of 
advancement.  Each  stage  should  be  studied  not  so  much  for 
itself,  as  for  the  evidence  it  affords  of  the  progress  of  develop- 
ment. In  the  study  of  embryology  it  does  not  suffice  to  acquire 
merely  a  series  of  *' still  pictures"  of  various  structures,  however 
accurate  these  pictures  may  be.  The  study  demands  a  constant 
application  of  correlative  reasoning  and  an  appreciation  of  the 
mechanical  factors  involved  in  the  relations  of  various  structures 
within  the  embryo  to  each  other,  and  in  the  relation  of  the 
embryo  as  a  whole  to  its  environment.  In  order  to  really 
comprehend  the  embryological  significance  of  a  structure  one 
must  know  not  only  its  relations  within  the  embryo  being 
studied  at  the  time,  but  also  the  manner  in  which  it  has  been 
derived  and  the  nature  of  the  changes  by  which  it  is  progressing 
toward  adult  conditions.  To  get  absolutely  the  whole  story  it  is 
obvious  that  one  would  have  to  study  a  series  of  embryos  with 
infinitely  small  intervals  between  them.  Nevertheless  the 
fundamental  steps  in  the  process  may  be  grasped  from  a  much 
less  extensive  series.  The  fewer  the  stages  studied,  however, 
the  more  careful  must  one  be  to  keep  in  mind  the  continuity 
of  the  processes  and  to  think  out  the  changes  by  which  one  stage 
leads  to  the  next. 

The  outstanding  idea  to  be  kept  in  mind  by  the  student  begin- 
ning the  study  of  embryology  is  that  the  development  of  an 
individual  is  a  process  and  that  this  process  is  continuous.  The 
conditions  he  sees  in  embryos  of  various  stages  are  of  importance 
chiefly  because  they  serve  as  evidence  of  events  in  the  process 
of  development  at  various  intervals  in  its  continuity,  as  his- 
torical events  are  evidences  of  the  progress  of  a  nation.  Just 
as  historical  events  are  led  up  to  by  preparatory  occurrences  and 
followed  by  results  which  in  turn  affect  later  events,  so  in  em- 
bryology events  in  development  are  presaged  by  preliminary 
changes  and  when  consummated  affect  in  turn  later  steps  in 
the  process. 

In  certain  respects  the  laboratory  study  of  embryological. 
material  involves  methods  of  work  for  which  courses  in  general 
zoology  do  not  entirely  prepare  the  student.  Some  general 
suggestions  as  to  methods  of  procedure  are,  therefore,  not  out 
of  place. 

In  dissecting  gross  material  it  is  not  unduly  difficult  to- 


4  EARLY   EMBRYOLOGY   OF   THE    CHICK 

appreciate  the  complete  relationships  of  a  structure.  The 
nature  of  embryological  material,  however,  introduces  new 
problems.  Embryos  of  the  age  when  the  establishment  of  the 
various  organ  systems  and  processes  of  body  formation  are  being 
initiated  are  too  small  to  admit  of  successful  dissection,  but 
npt  sufficiently  small  to  permit  of  the  satisfactory  micro- 
scopical study  of  an  entire  embryo,  except  for  its  more  general 
organization.  To  study  embryos  of  this  stage  with  any  degree 
of  thoroughness  they  must  be  cut  into  sections  which  are 
sufficiently  thin  to  allow  effective  use  of  the  microscope  to 
ascertain  cellular  organization  and  detailed  structural  relation- 
ships. In  preparing  such  material  the  entire  embryo  is  cut  into 
sections  which  are  mounted  on  slides  in  the  order  in  which 
they  were  cut.  A  sectional  view  of  any  region  of  the  embryo 
is  then  available  for  study. 

While  sections  readily  yield  accurate  information  about  local 
regions  it  is  extremely  difl&cult  to  construct  a  mental  picture 
of  any  whole  organism  from  a  study  of  serial  sections  alone. 
For  this  reason  it  is  necessary  to  work  first  on  entire  embryos 
which  have  been  prepared  by  staining  and  clearing  so  they  may 
be  studied  as  transparent  objects.  From  such  preparations 
it  is  possible  to  map  out  the  configuration  of  the  body,  and  the 
location  and  extent  of  the  more  conspicuous  internal  organs. 
In  this  work  the  fact  that  embryos  have  three  dimensions  must 
be  kept  constantly  in  mind  and  the  depth  at  which  a  structure 
lies  must  be  determined  as  well  as  its  apparent  position  in 
surface  view.  While  conventionally  entire  chick  embryos  are 
represented  in  dorsal  view,  much  additional  information  ma}^  be 
gained  by  following  a  study  of  the  dorsal,  with  a  study  of  the 
ventral  aspect.  Unless  the  preliminary  study  of  entire  embryos 
is  carefully  and  thoroughly  carried  out  the  study  of  sections 
will  yield  only  confusion. 

In  studying  a  section  of  an  embryo  it  is  necessary  first  of  all 
to  determine  its  location.  The  plane  of  the  section  under 
consideration,  and  the  region  of  the  embryo  through  which  it 
passes  should  be  ascertained  by  comparing  it  with  an  entire 
embryo  of  the  same  age  as  that  from  which  the  section  was  cut. 
Only  when  the  exact  location  of  a  section  is  known  can  the 
structures  appearing  in  it  be  correlated  with  the  organization  of 
the  embryo  as  a  whole.     Probably  nothing  in  the  study  of 


INTRODUCTION  5 

embryology  causes  students  more  difficulties  than  neglect  to 
locate  sections  accurately  with  the  consequent  failure  to  ap- 
preciate the  relationships  of  the  structures  seen  in  them.  Too 
great  emphasis  cannot  be  laid  on  the  vital  importance  of  fitting 
the  structures  shown  by  sections  properly  into  the  general 
scheme  of  organization  as  it  appears  in  whole-mounts.  It 
must  by  no  means  be  inferred  that  the  possibilities  of  the  whole- 
mounts  have  been  exhausted  by  the  preliminary  study  accorded 
them  before  taking  up  the  work  on  sections.  |  Further  and  more 
careful  study  of  entire  embryos  should  constantly  accompany 
the  study  of  serial  sections.  Many  details  which  in  the  initial 
observation  of  the  whole-mount  were  inconspicuous  or  abstruse 
will  become  significant  in  the  light  of  the  more  exact  information 
yielded  by  the  sections. 

In  the  discussion  of  structures  and  processes  in  embryology, 
it  is  necessary  to  use  terms  designating  location  and  direction 
which  are  referable  to  the  body  of  the  embryo  regardless  of  the 
position  it  occupies.  The  ordinary  terms  of  location,  which  are 
primarily  referred  to  the  direction  of  the  action  of  gravity, 
such  as  above,  over,  under  etc.  are  not  sufficiently  accurate. 
In  gross  human  anatomy,  there  still  persist  many  terms  that 
are  referred  to  gravity,  and  are  therefore,  because  of  the  erect 
posture  of  man,  not  applicable  to  comparative  anatomy  or  to 
embryology.  The  most  confusing  of  these  are  anterior  and 
posterior  as  used  in  gross  human  anatomy  to  mean,  respec- 
tively, pertaining  to  the  belly  and  to  the  back.  In  comparative 
anatomy  and  in  embryology,  anterior  has  reference  to  the  head 
region  and  posterior  to  the  tail  region.  The  use  of  these  terms 
in  embryology  in  the  sense  usual  in  gross  human  anatomy 
is  likely  to  lead  to  confusion  and  is  entirely  avoided  in  this 
book.  The  terms  anterior  and  posterior  have  been  replaced 
to  a  large  extent  by  their  less  confusing  synonyms,  cephalic 
and  caudal. 

In  addition  to  the  adjectives  of  position,  such  as  dorsal, 
ventral,  cephalic,  caudal,  mesial,  lateral,  proximal,  distal, 
corresponding  adverbs  of  motion  or  direction  are  commonly 
used  in  embryology.  These  adverbs  are  formed  by  adding  the 
suffix  -ad  to  the  root  of  the  adjective,  as  dorsad  meaning  toward 
the  back,  cephalad  meaning  toward  the  head,  etc.  These 
must  not  be  used  as  adjectives  of  position  but  should  be  ap- 


O  EARLY   EMBRYOLOGY   OF   THE   CHICK 

4 

plied  only  to  the  progress  of  processes,  or  to  the  extension  of 
structures  toward  the  part  indicated  by  the  root  of  the  adverb. 
Cultivation  of  the  use  of  correct  and  definite  terms  of  posi- 
tion and  direction  in  dealing  with  embryological  processes  will 
greatly  aid  accurate  thinking  and  clear  understanding. 


CHAPTER  II 

THE  GAMETES  AND  FERTILIZATION 

The  ovarian  ovum;  maturation,  ovulation,  and  fertiliza- 
tion;  THE   FORMATION   OF   THE   ACCESSORY   COVERINGS    OF 

THE  ovum;  the  structure  of  the  egg  at  the  time  of 
laying;  incubation. 

The  Ovarian  Ovum. — The  formation  of  the  ovum,  the  phe- 
nomena of  fertihzation,  and  the  stages  of  development  occurring 
prior  to  the  laying  of  the  egg  have  been  more  completely  worked 
out  in  the  pigeon  than  in  the  hen.  The  observations  which 
have  been  carried  out  on  the  hen's  egg  indicate,  as  might  be 
expected  from  the  near  relationship  of  the  pigeon  and  the  hen, 
that  the  processes  in  the  two  forms  are  closely  comparable. 
The  following  account  which  is  based  chiefly  on  observations 
made  on  the  pigeon's  egg  may,  therefore,  be  taken  to  apply 
equally  well  in  all  essentials  to  the  hen's  egg. 

The  part  of  the  egg  commonly  known  as  the  ''yolk"  is  a 
single  cell,  the  female  sex  cell  or  ovum.  Its  great  size  as  com- 
pared with  other  cells  is  due  to  the  food  material  it  contains. 
While  the  egg  cell  is  still  in  the  ovary,  material  which  is  later 
used  by  the  embryo  as  food  is  deposited  in  its  cytoplasm.  This 
deposit  which  is  known  as  deutoplasiii  consists  of  a  viscid  fluid 
in  which  are  suspended  granules  and  globules  of  Various  sizes. 
As  the  deutoplasm  increases  in  amount  the  nucleus  and  the  cyto- 
plasm are  forced  toward  the  surface  so  that  eventually  the 
deutoplasm  comes  to  occupy  nearly  the  entire  cell.  This 
abundance  of  deutoplasm  accumulated  in  the  ovum  furnishes 
a  readily  assimilable  food  supply,  which  makes  possible  the 
extremely  rapid  development  of  the  chick  embryo. 

A  section  of  the  hen's  ovary  passing  through  a  nearly  mature 
ovum  (Fig.  i)  shows  the  ovum  and  the  tissues  which  surround 
it  projecting  from  the  ovary  but  connected  to  it  by  a  constricted 
stalk  of  ovarian  tissue.  The  protuberance  containing  the  ovum 
is  known  as  a  follicle.     The  bulk  of  the  ovum  itself  is  made  up  of 

7 


8 


EARLY    EMBRYOLOGY   OF   THE    CHICK 


the  yolk.  Except  in  the  neighborhood  of  the  nucleus  the  active 
cytoplasm  is  but  a  thin  film  enveloping  the  yolk.  About 
the  nucleus  a  considerable  mass  of  cytoplasm  is  aggregated. 
The  region  of  the  ovum  containing  the  nucleus  and  the  bulk  of 
the  active  cytoplasm  is  known  as  the  animal  pole  because  this 
subsequently  becomes  the  site  of  greatest  protoplasmic  activity. 
The  region  opposite  the  animal  pole  is  called  the  vegetative 
pole  because  while  material  for  growth  is  drawn  from  this 
region  it  remains  itself  relatively  inactive. 


young  follicle 


connective  tissue 


stalk  of  follicle 


germinal  epithelium 
of  ovary 


white  yolk 


yellow  yolk 


cellular  (granular) 
zone  of  follicle 


theca  folliculi 


Fig.  I. — Diagram  showing  the  structure  of  a  bird  ovum  still  in  the  ovary. 
{Modified  from  Lillie,  after  Patterson.)  The  section  shows  a  follicle  containing 
a  nearly  mature  ovum,  together  with  a  small  area  of  the  adjacent  overian  tissue. 

Enclosing  the  ovum  is  a  thin  non-cellular  membrane,  the 
vitelline  membrane,  which  is  a  secretory  product  of  the  cyto- 
plasm of  the  ovum.  Outside  the  vitelHne  membrane  and  very 
difficult  to  differentiate  from  it,  is  another  secreted  membrane 
the  zona  radiata,  so  called  because  of  its  delicate  radial  stria- 
tions.  Immediately  peripheral  to  the  zona  radiata  is  an  invest- 
ment of  small  polygonal  cells,  the  cellular  or  ** granular"  zone 
of  the  follicle,  which  is  in  turn  enclosed  in  a  highly  vascular 
coat  of  connective  tissue,  the  theca  folliculi.  The  nutriment 
for  the  growing  ovum  is  supplied  by  the  mother  from  the  prod- 


GAMETES   AND  FERTILIZATION 


ucts  of  her  digested  food.  It  is  brought  in  through  the  blood 
vessels  of  the  theca,  absorbed  by  the  follicular  cells  and  trans- 
ferred by  them  to  the  ovum.  Within  the  ovum  this  material  is 
elaborated  into  deutoplasm. 

Maturation,  Ovulation  and  Fertilization. — When  the  full 
allotment  of  deutoplasm  has  accumulated  in  the  ovum  the 
nucleus  undergoes  its  first  maturation  division.  Maturation 
is  a  process  occurring  before  fertilization,  in  which  there  is 
an  equal  mitotic  division  of  the  nucleus  of  the  ovum  but  a 
markedly  unequal  division  of  the  cytoplasm  and  its  contents. 
y  The  result  of  this  division  is  the  formation  of  one  very  large  cell 
containing  the  entire  dower  of  deutoplasm  and  one  very  small 
cell  containing  practically  no  deutoplasm.  This  small  cell  is  call- 
ed a  polar  body  because  it  is  budded  off  at  the  animal  pole  of  the 
ovum.  Since  this  unequal  division  of  the  ovum  typically 
occurs  twice  we  speak  of  the  first  and  second 
maturation  divisions  and  of  the  first  and  second 
polar  bodies. 

In  one  of  these  maturation  divisions  the 
chromosomes  do  not  split  at  the  metaphase  stage 
as  happens  in  ordinary  mitoses.  Instead,  half  of 
the  original  number  of  chromosomes  migrate 
bodily  to  each  pole  of  the  spindle,  with  the  result 
that  each  daughter  nucleus  receives  but  half  the 
number  of  chromosomes  normal  for  the  somatic 
cells  of  the  species.  Such  a  modified  mitotic 
division  is  known  as  a  reduction  division.  After 
the  maturation  divisions,  one  of  which  is  a  reduc- 
tion division,  the  nucleus  of  the  ovum  now  ready 
for  fertilization,  is  called  the  female  pronucleus. 

Although  maturation  in  the  male  sex  cells 
differs  in  some  respects  from  the  maturation  of 
the  ovum,  there  also,  a  reduction  division  occurs. 
The  result  is  that  the  nucleus  of  each  matured 
cell  contains  but  half  the  species  number  of  chromo- 
somes. When  in  the  process  of  fertilization  the  nucleus  of  the 
male  cell  unites  with  the  female  pronucleus  the  full  species 
number  of  chromosomes  is  restored. 

At  about  the  time  of  the  first  maturation  division  the  follicle 
ruptures,  and  the  liberated  ovum  passes  into  the  oviduct.     If 


Fig.  2.— 
S  permatozoon 
of  the  pigeon. 
(After  Ballo- 
witz.) 


lO  EARLY  EMBRYOLOGY  OF  THE  CHICK 

insemination  has  taken  place  meanwhile,  the  spermatozoa 
(Fig.  2)  make  their  way  along  the  oviduct  where  for  several 
days  they  may  remain  alive  and  capable  of  performing  their 
function  of  fertilization.  Penetration  of  the  ovum  by  sperma- 
tozoa takes  place  in  the  region  of  the  oviduct  near  the  ovary, 
before  the  albumen  and  shell  have  been  added  to  the  ovum. 
Coincidently  the  second  polar  body  is  extruded.  Although  in 
birds  normally  several  spermatozoa  penetrate  the  ovum,  only  a 
single  one  unites  with  the  female  pronucleus.  The  fusion  of  the 
male  and  female  pronuclei  in  fertilization  initiates  the  develop- 
ment of  the  embryo  and  the  cleavage  divisions  are  begun  while 
the  ovum  is  passing  through  the  oviduct  toward  the  cloaca  and 
receiving  meanwhile  its  accessory  coverings. 

The  Formation  of  the  Accessory  Coverings  of  the  Ovum. 
The  albumen,  the  shell  membrane,  and  the  shell  are  non-cellular 
investments  secreted  about  the  ovum  by  the  cells  lining  the 
oviduct.  In  the  part  of  the  oviduct  adjacent  to  the  ovary  a 
mass  of  stringy  albuminous  material  is  produced.  This  ad- 
heres closely  to  the  vitelline  membrane  and  projects  beyond 
it  in  two  masses  extending  in  either  direction  along  the  oviduct. 
Due  to  the  spirally  arranged  folds  in  the  walls  of  the  oviduct, 
the  egg  as  it  moves  toward  the  cloaca  is  rotated.  This  rotation 
twists  the  adherent  albumen  into  the  form  of  spiral  strands  pro- 
jecting at  either  end  of  the  yolk,  known  as  the  chalazae  (Fig. 
3).  Additional  albumen,  which  has  been  secreted  abundantly 
in  advance  of  the  ovum  by  the  glandular  lining  of  the  oviduct, 
is  caught  in  the  chalazae  and  during  the  further  descent  of  the 
ovum  is  wrapped  about  it  in  concentric  layers.  These  lamellae 
of  albumen  may  be  easily  demonstrated  in  an  egg  which  has  had 
the  albumen  coagulated  by  boiling.  The  albumen  secreting 
region  of  the  oviduct  constitutes  about  one-half  of  its  entire 
length. 

The  shell  membranes  which  consist  of  sheets  of  matted 
organic  fibers  are  added  farther  along  in  the  oviduct.  The 
shell  is  secreted  as  the  egg  is  passing  through  the  shell  gland 
portion  of  the  oviduct.  The  entire  passage  of  the  ovum  from 
the  time  of  its  discharge  from  the  ovary  to  the  time  when  it  is 
ready  for  laying  has  been  estimated  to  occupy  about  22  hours. 
If  the  completely  formed  egg  reaches  the  cloacal  end  of  the 
oviduct  during  the  middle  of  the  day  it  is  usually  laid  at  once, 


GAMETES    AND. FERTILIZATION  II 

otherwise  it  is  likely  to  be  retained  until  the  following  day. 
This  over  night  retention  of  the  egg  is  one  of  the  factors  which 
accounts  for  the  variability  in  the  stage  of  development  reached 
at  the  time  of  laying. 

The  Structtire  of  the  Egg  at  the  Time  of  Laying. — The 
arrangement  of  structures  in  the  egg  at  the  time  of  laying 
is  shown  in  Figure  3.  Most  of  the  gross  relationships  are 
already  familiar  because  they  appear  so  clearly  in  eggs  which 
have  been  boiled.  If  a  newly  laid  egg  is  allowed  to  float  free 
in  water  until  it  comes  to  rest  and  is  then  opened  by  cutting 

nucleus  of  Pander         _  blastoderm 

neck  of  latebra 


white  yolk  ^^55^..^  ^»^^^^v  less  dense  albumen 

yeUow  yolk^  'vitelline  membrane 

Pig.  3. — Diagram  of  the  hen's  egg  in  longitudinal  section.  (After  Lillie.) 
The  relations  of  the  various  parts  of  the  egg  at  the  time  of  laying  are  indicated 
schematically. 

away  the  part  of  the  shell  which  lies  uppermost,  a  circular 
whitish  area  will  be  seen  to  lie  atop  the  yolk.  In  eggs  which 
have  been  fertilized  this  area  is  somewhat  different  in  appear- 
ance and  noticeably  larger  than  it  is  in  unfertilized  eggs.  The 
differences  are  due  to  the  development  which  has  taken  place  in 
fertilized  eggs  during  their  passage  through  the  oviduct.  The 
aggregation  of  cells  which  in  fertilized  eggs  lies  in  this  area  is 
known  as  the  blastoderm.  The  structure  of  the  blastoderm  and 
the  manner  in  which  it  grows  will  be  taken  up  in  the  next 
chapter. 

Close  examination  of  the  yolk  will  show  that  it  is  not  uniform 
throughout  either  in  color  or  in  texture.     Two  kinds  of  yolk 


12  EARLY   EMBRYOLOGY   OF   THE    CHICK 

can  be  differentiated,  white  yolk,  and  yellow  yolk.  Aside  from 
the  difference  in  color  visible  to  the  unaided  eye,  microscopical 
examination  will  show  that  there  are  differences  in  the  granules 
and  globules  of  the  two  types  of  yolk,  those  in  the  white  yolk 
being  in  general  smaller  and  less  uniform  in  appearance.  The 
principal  accumulation  of  white  yolk  lies  in  a  central  flask- 
shaped  area,  the  latebra,  which  extends  toward  the  blastoderm 
and  flares  out  under  it  into  a  mass  known  as  the  nucleus  of 
Pander.  In  addition  to  the  latebra  and  the  nucleus  of  Pander 
there  are  thin  concentric  layers  of  white  yolk  between  which  lie 
much  thicker  layers  of  yellow  yolk.  The  concentric  layers  of 
white  and  yellow  yolk  are  said  to  indicate  the  daily  accumula- 
tion of  deutoplasm  during  the  final  stages  in  the  formation  of 
the  egg.  The  outermost  yolk  immediately  under  the  vitelline 
membrane  is  always  of  the  white  variety. 

The  albumen,  except  for  the  chalazae,  is  nearly  homogeneous 
in  appearance,  but  near  the  yolk  it  is  somewhat  more  dense 
than  it  is  peripherally.  The  chalazae  serve  to  suspend  the  yolk 
in  the  albumen. 

The  two  layers  of  shell  membrane  lie  in  contact  everywhere 
except  at  the  large  end  of  the  egg  where  the  inner  and  outer 
membranes  are  separated  to  forni  an  air  chamber.  This 
space  is  stated  (Kaupp)  to  appear  only  after  the  egg  has 
been  laid  and  cooled  from  the  body  temperature  of  the  hen 
(about  io6°F.)  to  the  ordinary  temperatures.  In  eggs  which 
have  been  kept  for  any  length  of  time  the  air  space  increases 
in  size  due  to  evaporation  of  part  of  the  water  content  of 
the  egg.  This  fact  is  taken  advantage  of  in  the  familiar  method 
of  testing  the  freshness  of  eggs  by  "floating  them." 

The  egg  shell  is  composed  largely  of  calcareous  salts.  These 
salts  are  derived  from  the  food  of  the  mother  and  if  lime  con- 
taining substances  are  not  furnished  in  her  diet  the  shell  is 
defectively  formed  or  even  altogether  wanting.  The  shell  is 
porous  allowing  the  embryo  to  carry  on  exchange  of  gases  with 
the  outside  air  by  means  of  specialized  vascular  membranes 
arising  in  connection  with  the  embryo  but  lying  outside  it, 
directly  beneath  the  shell. 

Incubation. — When  an  egg  has  been  laid,  development  ceases 
unless  the  temperature  of  the  egg  is  kept  nearly  up  to  the  body 
temperature  of  the  mother.     Cooling  of  the  egg  does  not,  how- 


GAMETES   AND    FERTILIZATION  13 

ever,  lesult  in  the  death  of  the  embryo.  It  may  resume  its 
development  if  it  is  brooded  by  the  hen  or  artificially  incubated 
even  after  the  egg  has  been  kept  for  many  days  at  ordinary 
temperatures. 

The  normal  incubation  temperature  is  that  at  which  the  egg 
is  maintained  by  the  body  heat  from  the  brood-hen.  This  is 
somewhat  below  the  blood  heat  of  the  hen  (io6°F.).  When  an 
egg  is  allowed  to  remain  undisturbed  the  yolk  rotates  so  that 
the  developing  embryo  lies  uppermost.  Its  position  is  then 
such  that  it  gets  the  full  benefit  of  the  warmth  of  the  mother. 

In  incubating  eggs  artificially  the  incubators  are  usually 
regulated  for  a  heat  of  ioo°-ioi°F.  (37°-38°C.).  At  this 
temperature  the  chick  is  ready  for  hatching  on  the  twenty-first 
day.  Development  will  go  on  at  considerably  lower  tempera- 
tures but  its  rate  is  retarded  in  proportion  to  the  lowering  of  the 
temperature.  Below  about  21  degrees  Centigrade  develop- 
ment ceases  altogether. 

In  incubating  eggs  which  have  been  cooled  after  laying  for 
some  particular  stage  of  the  embryo  which  it  is  desired  to  secure, 
three  or  four  hours  are  ordinarily  allowed  for  the  egg  to  become 
warmed  to  the  point  at  which  development  begins  again.  For 
example  if  an  embryo  of  24-hours  incubation  age  is  desired  the 
egg  should  be  allowed  to  remain  in  the  incubator  about  27  hours. 
Even  with  allowance  made  for  the  warming  of  the  egg  and  with 
exact  regulation  of  the  temperature  of  the  incubator,  the  stage  of 
development  attained  in  a  given  incubation  time  will  vary 
widely  in  different  eggs.  The  factor  of  individual  variabiHty 
which  must  always  be  reckoned  with  in  developmental  proces- 
ses, undoubtedly  accounts  for  some  of  the  variation.  The 
different  time  occupied  by  different  eggs  in  traversing  the  ovi- 
duct, the  over-night  retention  of  eggs  not  ready  for  laying  till 
toward  sundown,  and  especially  the  varying  time  different  eggs 
have  been  brooded  before  being  removed  from  the  nest,  account 
for  further  variations.  The  designation  of  the  age  of  chicks  in 
hours  of  incubation  is,  therefore,  not  exact,  but  merely  a  con- 
venient approximation  of  the  average  condition  reached  in 
that  incubation  time. 


CHAPTER  III 

THE  PROCESS  OF  SEGMENTATION 

The  effect  of  yolk  on  segmentation;  the  unsegmented 
blastodisc;  the  sequence  and  orientation  of  the 
cleavage  division  in  birds. 

The  Effect  of  Yolk  on  Segmentation. — Immediately  after 
its  fertilization  the  ovum  enters  upon  a  series  of  mitotic  divisions 
which  occur  in  close  succession.  This  series  of  divisions 
constitutes  the  process  of  segmentation  or  cleavage.  In  birds 
segmentation  takes  place  before  the  egg  is  laid,  during  the  time 
it  is  traversing  the  oviduct. 

A  mitotic  division,  whether  it  be  a  cleavage  division  of  the 
ovum  or  the  division  of  some  other  cell,  is  carried  out  by  the 
active  protoplasm  of  the  cell.  The  food  material  stored  in  an 
egg  cell  as  deutoplasm  is  non-living  and  inert.  The  deutoplasm 
has  no  part  in  mitosis  except  as  its  mass  mechanically  influences 
the  activities  of  the  protoplasm  of  the  cell.  It  is  obvious  that 
any  considerable  amount  of  yolk  will  retard  the  division,  or 
prevent  the  complete  division,  of  the  fertilized  ovum.  The 
amount  and  distribution  of  the  yolk  will  therefore  determine 
the  type  of  segmentation. 

Figure  4  shows  diagrammatically  the  manner  in  which  the 
first  cleavage  division  is  carried  out  in  three  types  of  eggs 
having  different  relative  amounts  and  different  distributions  of 
yolk  and  protoplasm.  In  the  egg  of  Amphioxus  the  yolk  is 
relatively  meager  in  amount  and  fairly  uniformly  distributed 
throughout  the  cell.  An  ovum  with  such  a  yolk  distribution  is 
termed  isolecithal  (homolecithal).  An  isolecithal  egg  under- 
goes a  type  of  cleavage  which  is  essentially  an  unmodified 
mitosis.  The  yolk  is  not  sufficient  in  amount,  nor  sufficiently 
localized  to  alter  the  usual  mode  of  cell  division. 

In  Amphibia  the  ovum  contains  a  considerable  amount 
of  yolk  and  the  accumulation  of  the  yolk  at  one  pole  has  crowded 
the  nucleus  and  active  cytoplasm  of  the  ovum  toward  the 
opposite  pole.     An  egg  in  which  the  yolk  is  thus  concentrated 

14 


PROCESS   OF   SEGMENTATION 


15 


at  one  pole  is  termed  telolecithal.     Cleavage  in  such  an  egg  is 
initiated  at  the  animal  pole  where  the  nucleus  and  most  of  the 


Q  -g 

3  -^ 

<^  > 

O  rt 

to  o 

O  43 


iG 


z 

O  Xi 

<  a 

w  ° 

3  "s 


active  cytoplasm  are  located.  The  division  of  the  nucleus  is  a 
typical  mitotic  division.  The  division  of  the  cytoplasm  is 
effected  rapidly  at  the  animal  pole  of  the  egg  where  the  active 


1 6  EARLY   EMBRYOLOGY   OF   THE   CHICK 

cytoplasm  is  aggregated.  When,  however,  the  yolk  mass  is 
encountered,  the  process  is  greatly  retarded.  So  slowly,  in 
fact,  is  the  division  of  the  yolk  accomplished,  that  succeeding 
cell  divisions  begin  at  the  animal  pole  of  the  egg  before  the  first 
cleavage  is  completed  at  the  vegetative  pole. 

The  eggs  of  birds  are  also  telolecithal,  but  the  amount  of 
yolk  which  they  contain  is  both  relatively  and  actually  much 
greater  than  that  in  Amphibian  eggs.  Cleavage  in  bird's  eggs 
begins  as  it  does  in  the  eggs  of  Amphibia,  but  the  mass  of  the 
inert  yolk  material  in  them  is  so  great  that  the  yolk  is  not 
divided.  The  process  of  segmentation  is  limited  to  the  small 
disc  of  protoplasm  lying  on  the  surface  of  the  yolk  at  the  animal 
pole,  and  is  for  this  reason  referred  to  as  discoidal  cleavage 
(Fig.  5).  The  fact  that  the  whole  egg  is  not  divided  is  indicated 
by  designating  the  process  as  partial  (meroblastic)  cleavage 
in  distinction  to  the  complete  cleavage  (holoblastic)  seen  in 
eggs  containing  less  yolk.  The  cells  formed  in  the  process  of 
segmentation  are  known  as  blastomeres  whether  they  are  com- 
pletely separated  as  results  in  holobastic  cleavage  or  only 
partially  separated  as  results  in  meroblastic  cleavage. 

The  Unsegmented  Blastodisc. — In  the  egg  of  a  bird  which  is 
about  to  undergo  cleavage,  the  disc  of  active  protoplasm  at  the 
animal  pole  (blastodisc)  is  a  whitish,  circular  area  about  three 
millimeters  in  diameter.  The  central  portion  of  the  blastodisc 
is  surrounded  by  a  somewhat  darker  appearing  marginal  area 
known  as  the  periblast.  The  protoplasm  of  the  blastodisc, 
especially  in  the  periblast  region,  blends  into  the  underlying 
white  yolk  so  that  it  is  difficult  to  make  out  any  line  of  demarca- 
tion between  the  two.  It  is  in  the  central  area  of  the  blasto- 
disc that  cleavage  furrows  first  appear.  Neither  the  nuclei 
resulting  from  the  early  cleavages  nor  the  cleavage  furrows 
invade  the  marginal  periblast  until  very  late  in  the  process  of 
segmentation. 

The  Sequence  and  Orientation  of  the  Cleavage  Divisions  in 
Birds. — The  nature  of  the  series  of  divisions  in  the  meroblastic, 
discoidal  cleavage  characteristic  of  the  eggs  of  birds  is  largely 
determined  by  the  amount  and  distribution  of  the  yolk.  An- 
other determining  factor  is  the  tendency  of  mitotic  spindles  to 
develop  so  that  the  long  axis  of  the  spindle  lies  at  right  angles 
to  the  axis  of  least  dimension  of  the  mass  of  unmodified  cyto- 
plasm.    The  cleavage  furrow  always  arises  at  right  angles  to 


PROCESS    OF    SEGMENTATION  1 7 

the  long  axis  of  the  mitotic  spindle.  Figure  5  shows  the  succes- 
sion of  the  cleavage  divisions  in  the  egg  of  the  pigeon.  The 
diagrams  represent  surface  views  of  the  blastodisc  and  an  area 
of  the  surrounding  yolk,  the  shell  and  albumen  having  been 
removed.  The  observer  is  looking  directly  at  the  animal  pole. 
Figure  5,  ^,  should  be  compared  with  Figure  4.  The  diagrams 
of  Figure  4  are  of  sections  cut  in  a  plane  which  passes  vertically 
through  the  blastodisc  and  which  is  at  right  angles  to  the  plane 
of  the  first  cleavage  (Fig.  5,  A,  I-I).  The  first  cleavage  furrow 
cuts  into  the  egg  in  a  plane  coinciding  with  the  imaginary  axis 
passing  through  the  animal  pole  and  the  vegetative  pole.  The 
two  daughter  cells  or  blastomeres  resulting  from  the  first 
cleavage  are  not  completely  walled  off  but  each  remains 
unseparated  from  the  underlying  yolk  (Fig.  4). 

In  each  of  the  two  blastomeres  resulting  from  the  first  cleav- 
age division,  mitotic  spindles  initiating  the  second  cleavage  arise 
at  right  angles  to  the  position  which  was  occupied  by  the  first 
cleavage  spindle.  This  determines  that  the  two  second  cleav- 
age furrows  will  be  at  right  angles  to  the  first.  Since  these 
two  second  cleavage  furrows  lie  in  the  same  plane  and  are 
apparently  continuous  they  are  usually  considered  together. 
They  mark  the  position  of  the  second  cleavage  plane  which  cuts 
the  egg  in  the  animal- vegetative  axis  but  which  lies  at  right 
angles  to  the  first  cleavage  plane  (Fig.  5,  B,  II-II).  A  very 
good  way  of  getting  a  clear  conception  of  the  orientation  of  the 
ojeavage  planesJs  to  cut  them  in  an  apple.  Let  the  core  of  the 
apple  represent  the  animal- vegetative  axis  of  the  egg.  The  first 
cleavage  furrow  can  be  represented  by  notching  the  apple 
lengthwise,  that  is  as  one  ordinarily  starts  to  split  an  apple  into 
halves.  The  second  cleavage  furrow  can  be  represented  by 
cutting  into  the  apple  again  in  a  plane  passing  through  the 
axis  of  the  core,  but  at  right  angles  to  the  first  cut,  as  one  would 
start  to  quarter  the  apple. 

The  third  cleavage  furrows  are  variable  in  number  and  in 
position.  In  the  most  typical  cases  each  of  the  four  blastomeres 
established  by  the  first  two  cleavages  divides  again  so  that  eight 
blastomeres  are  formed  (Fig.  5,  C).  Frequently,  however,  the 
third  cleavage  appears  at  first  in  only  two  of  the  blastomeres, 
so  that  six  cells  result  instead  of  eight. 

The  fourth  series  of  cleavages  takes  place  in  such  a  manner 


i8 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


Fig.  5. — Surface  aspect  of  blastoderm  at  various  stages  of  cleavage.  {Based 
on  Blount's  photomicrographs  of  the  pigeon's  egg.)  The  blastodenn  and  the 
immediately  surrounding  yolk  are  viewed  directly  from  the  animal  pole,  the 
shell  and  albumen  having  been  removed.  The  order  in  which  the  cleavage 
furrows  have  appeared  is  indicated  on  the  diagrams  by  Roman  numerals. 

A,  first  cleavage;  B,  second  cleavage;  C,  third  cleavage;  D,  fourth  cleavage; 
£,  fifth  cleavage;  F,  early  morula. 


PROCESS    OF    SEGMENTATION  IQ 

that  the  central  (apical)  ends  of  the  eight  cells  established  by 
the  third  cleavage  are  cut  off  from  their  peripheral  portions. 
The  combined  contour  of  the  fourth  cleavage  furrows  forms  a 
small  irregularly  circular  furrow  the  center  of  which  is  the  point 
at  which  the  first  two  cleavage  planes  intersect  (Fig.  5,  D). 
The  central  cells  now  appear  completely  separated  in  a  surface 
view  of  the  blastoderm,  but  sections  show  them  still  unseparated 
from  the  underlying  yolk. 

After  the  fourth,  the  succession  of  cleavages  becomes  irregular. 
In  surface  view  it  is  possible  to  make  out  cleavage  furrows  that 
divide  off  additional  apical  cells,  and  other,  radial  furrows  that 
further  divide  the  peripheral  cells.  Figure  5,  E  and  F,  show  the 
increase  in  number  of  cells  and  their  extension  out  over  the 
surface  of  the  yolk,  resulting  from  the  succession  of  cleavages. 
When  the  process  of  segmentation  has  progressed  to  the  stage 
in  which  the  succession  of  cleavages  is  irregular  and  the  number 
of  cells  considerable,  the  term  blastoderm  is  applied  to  the  entire 
group  of  blastomeres  formed  by  the  cleavage  of  the  blastodisc.^ 

In  addition  to  the  cleavages  which  are  indicated  on  the  sur- 
face, at  about  the  3  2 -cell  stage  sections  show  cleavage  planes  of 
an  entirely  different  character.  These  cleavages  appear  below 
the  surface  and  parallel  to  it.  They  establish  a  superficial  layer 
of  cells  which  are  completely  delimited.  These  superficial 
cells  rest  upon  a  layer  of  cells  which  are  continuous  on  their  deep 
faces  with  the  yolk.  Continued  divisions  of  the  same  type 
eventually  establish  several  strata  of  superficial  cells.  This 
process  appears  first  in  the  central  portion  of  the  blastoderm. 
It  progresses  centrifugally  as  the  blastoderm  increases  in  size 
but  does  not  extend  to  its  extreme  margin.  The  peripheral 
margin  of  the  blastoderm  remains  a  single  cell  in  thickness  and 
the  cells  there  lie  unseparated  from  the  yolk. 

1  While  but  a  single  spermatozoon  takes  part  in  fertilization  other  spermatoza 
become  lodged  in  the  cytoplasm  of  the  blastodisc.  The  nuclei  of  these  sperma- 
tozoa migrate  to  the  peripheral  part  of  the  blastoderm  where  they  are  recog- 
nizable for  some  time  as  the  so-called  accessory  sperm  nuclei.  Some  of  them 
appear  to  undergo  divisions  which  are  accompanied  by  slight  indications  of 
division  in  the  adjacent  cytoplasm.  The  short  superficial  grooves  thus  formed 
are  termed  accessory  cleav^age  furrows.  No  cells  are  formed  by  the  accessory 
"cleavages."  The  sperm  nuclei  soon  degenerate,  the  superficial  furrows  fade 
out,  and  usually  as  early  as  the  3  2 -cell  stage  all  traces  of  the  process  have  dis- 
appeared without,  as  far  as  is  known,  affecting  in  any  way  the  development  of 
the  embryo. 


CHAPTER  IV 
THE  ESTABLISHMENT  OF  THE  ENTODERM 

The  morula  stage;  the  formation  of  the  blastula;  the 
effect  of  yolk  on  gastrulation ;  gastrulation  in 

BIRDS. 

The  Morula  Stage. — It  should  by  no  means  be  inferred  that 
cell  division  ceases  with  the  cleavage  divisions.  The  end  of  the 
segmentation  stage  is  not  marked  by  even  a  retardation  in  the 
succession  of  mitoses.  Segmentation  is  regarded  as  ending  when 
the  progress  of  development  ceases  to  be  indicated  merely  by 
increases  in  the  number  of  cells,  and  begins  to  involve  locaHzed 
aggregation  and  differentiation  of  various  groups  of  cells. 
Development  progresses  from  phase  to  phase  without  abrupt 
change  or  interruption.  The  nomenclature  and  limitation  of 
the  various  phases  of  development  are  largely  arbitrary  and  the 
use  of  terms  designating  phases  or  stages  of  development  should 
not  be  allowed  to  obscure  the  fact  that  the  whole  process  is  a 
continuous  one. 

In  eggs  without  a  large  amount  of  yolk,  segmentation  results 
in  the  formation  of  a  rounded,  closely  packed  mass  of  blasto- 
meres.  This  is  known  as  a  morula  from  its  resemblance  to  the 
mulberry  fruit  which  is  in  form  much  like  the  more  familiar 
raspberry  or  blackberry.  At  the  end  of  segmentation  the 
chick  embryo  has  arrived  at  a  stage  which  corresponds  with  the 
morula  stage  of- forms  with  less  yolk.  It  consists  of  a  disc- 
shaped mass  of  cells  several  strata  in  thickness,  the  blastoderm, 
lying  closely  appUed  to  the  yolk.  In  the  center  of  the  blasto- 
derm the  cells  are  smaller  and  completely  defined;  at  the  per- 
iphery the  cells  are  flattened,  larger  in  surface  extent,  and  are 
not  walled  off  from  the  yolk  beneath. 

The  Formation  of  the  Blastula. — The  morula  condition  is  of 
short  duration.  Almost  as  soon  as  it  is  established  there  begins 
a  rearrangement  of  the  cells  presaging  the  formation  of  the 
blastula.     A  cavity  is  formed  beneath  the  blastoderm  by  the 

20 


ESTABLISHMENT    OF    THE    ENTODERM  21 

detachment  of  its  central  cells  from  the  underlying  yolk  while 
the  peripheral  cells  remain  attached.  The  space  thus  estab- 
lished between  the  blastoderm  and  the  yolk  is  termed  the  seg- 
mentation cavity  (blastocoele).  The  marginal  area  of  the 
blastoderm  in  which  the  cells  remain  undetached  from  the  yolk  , 
and  closely  adherent  to  it,  is  called  the  zone  of  junction.  With 
the  establishment  of  the  blastocoele  the  embryo  is  said  to  have 
progressed  from  the  morula  to  the  blastula  stage. 

Figure  7,  D,  shows  the  conditions  seen  on  sectioning  the 
blastula  of  a  bird.  Only  the  blastoderm  and  the  immediately 
underlying  yolk  are  included  in  the  diagram.  At  this  mag- 
nification the  complete  yolk  must  be  imagined  as  about  three 
feet  in  diameter.  The  structure  of  the  bird  embryo  in  these 
stages  may  be  brought  in  line  with  the  morula  and  blastula 
stages  of  forms  having  little  yolk  if  the  full  significance  of  the 
great  yolk  mass  is  appreciated.  Instead  of  being  free  to  aggre- 
gate first  into  a  solid  sphere  of  cells  (morula)  and  then  into  a 
hollow  sphere  of  cells  (blastula),  as  takes  place  in  forms  with  ^ 
little  yolk,  the  blastomeres  in  the  bird  embryo  are  forced 
to  grow  on  the  surface  of  a  large  yolk  sphere.  Under 
such  mechanical  conditions  the  blastomeres  are  forced  to  be- 
come arranged  in  a  disc-shaped  mass  on  the  surface  of  the  yolk. 
If  one  imagines  the  yolk  of  the  bird  morula  removed,  and  the 
disc  of  cells  left  free  to  assume  the  spherical  shape  dictated  by 
surface  tension  its  comparability  with  the  morula  in  a  form 
having  little  yolk  becomes  apparent. 

The  process  of  blastulation  also  is  modified  by  the  presence 
of  a  large  amount  of  yolk.  There  can  be  no  simple  hollow 
sphere  formation  by  rearrangement  of  the  cells  if  the  great 
bulk  of  the  morula  is  inert  yolk.  But  the  cells  of  the  central 
region  of  the  blastoderm  are  nevertheless  separated  from  the 
yolk  to  form  a  small  blastocoele.  The  yolk  constitutes  the 
floor  of  the  blastocoele  and  at  the  same  time  by  reason  of  its. 
great  mass  nearly  obliterates  it.  If  we  imagine  the  yolk 
removed  from  the  blastula  and  the  edges  of  the  blastoderm 
pulled  together  the  chick  blastula  approaches  the  form  of  the 
blastula  in  embryos  with  little  yolk. 

The  Effect  of  Yolk  on  Gastnxlation. — The  process  of  gastrula-  -^ 
tion  begins  as  soon  as  blastulation  is  accompHshed.     Gastrula- 
tion  as  it  occurs  in  birds  is  not  difiicult  to  understand  if  one 


22 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


grasps  its  fundamental  similarity  to  the  corresponding  process 
in  forms  with  scanty  yolk.  In  Amphioxus,  gastrulation  is  an 
inpocketing  of  the  blastula  (Fig.  6).  A  double  layered  cup  is 
formed  from  a  single  layered  hollow  sphere  much  as  one  might 


GASTRULATION   IN   PORM   WITH   ISOLECITHAL   EGG  HAVING  ALMOST  NO  YOLK— AMPHIOXU& 


GASTRULATION  IN  FORM  WITH  TELOLECITHAL  EGG  CONTAINING  MODERATE 
AMOUNT  OF  YOLK— AMPHIBIA. 


GASTRULATION  IN  FORM  WITH  TELOLECITHAL  EGG  CONTAINING  LARGE 
AMOUNT  OF  YOLK— BIRDS. 

Auu^^'  .^•~S<^^^"^atic  diagrams  to  show  the  effect  of  yolk  on  gastrulation. 
Abbreviations:  blc,  blastocoele;  bid.,  blastoderm;  blp.,  blastopore;  ect.,  ectoderm; 
ent.,  entoderm;  mit.,  cell  undergoing  mitosis;  yk.,  yolk;  vk.g.,  yolk  granules: 
yk.p..  yolk  plug. 

push  in  a  hollow  rubber  ball  with  the  thumb.  The  new  cavity 
in  the  double  walled  cup  is  termed  the  gastrocoele.  The  open- 
inir  from  the  outside  into  the  gastrocoele  is  called  the  blastopore. 


ESTABLISHMENT    OF    THE    ENTODERM  23 

In  gastrulation  the  single  cell  layer  of  the  blastula  is  doubled 
upon  itself  to  form  two  layers.  The  outer  cell  layer  is  known 
as  the  ectoderm  and  the  inner  layer  as  the  entoderm.  These 
layers  differ  from  each  other  in  their  positional  relationship  to 
the  embryo  and  to  the  surrounding  environment.  Each  has 
different  functional  potentiaHties  and  each  will  in  the  course  of 
development  give  rise  to  quite  different  types  of  structures  and 
organs.  It  is  the  importance  of  their  later  history  rather  than 
any  complexity  or  veiled  significance  about  the  way  in  which 
they  arise  that  attaches  such  importance  in  embryology  to  the 
establishment  of  these  two  layers. 

In  the  gastrulation  of  Amphibian  embryos  (Fig.  6)  the  yolk 
forces  the  invagination  of  the  blastoderm  toward  the  animal 
pole,  but  the  inpocketing  takes  place  into  the  blastocoele  and 
the  interrelationships  of  ectoderm,  entoderm,  and  gastrocoele 
are  established  in  fundamentally  the  same  way  as  in  Amphioxus. 

Gastrulation  in  birds  is  greatly  modified  by  the  large  amount 
of  yolk  present  (Fig.  6).  Infolding  must  be  effected  in  a  disc 
of  cells  resting  like  a  cap  on  a  large  yolk  sphere.  The  smallness 
of  the  blastocoele  sharply  restricts  the  space  into  which  the 
invagination  can  grow.  Instead  of  arising  as  a  relatively 
large  circular  opening  the  blastopore  appears  as  a  crescentlc 
slit  at  the  margin  of  the  blastoderm.  The  crescentic  blastopore 
may  be  regarded  as  a  potejitially  circular  opening  which  has 
been  flattened  as  it  develops  between  the  growing  disc  of  cells 
and  the  unyielding  yolk  which  underhes  them.  The  invagi- 
nated  pocket  of  entoderm  which  grows  in  from  this  compressed 
blastopore  is  also  flattened,  conforming  to  the  restrictions 
of  the  shape  and  size  of  the  blastocoele.  Moreover  the  floor 
of  the  invagination  is  represented  only  by  a  few  widely  scattered 
cells  lying  upon  the  yolk.  It  is  as  if  the  lower  layer  in  its  in- 
growth was  impeded  and  broken  up  by  the  yolk.  The  scattered 
cells  representing  the  floor  of  the  invagination  soon  disappear  and 
the  yolk  itself  comes  to  constitute  the  floor  of  the  gastrocoele. 
Notwithstanding  the  great  displacement  of  the  blastopore  and 
the  gastrular  invagination  toward  the  animal  pole  ajid  the 
restricted  size  and  incomplete  floor  of  the  gastrocoele,  the  cell 
layers  and  the  cavity  established  can  be  homologized  with  the 
corresponding  features  in  forms  where  the  course  of  develop- 
ment has  not  been  so  extensively  modified  by  yolk. 


24  EARLY   EMBRYOLOGY    OF    THE    CHICK 

A  comparative  review  of  the  diagrams  of  Figure  6  will  afford 
a  general  understanding  of  the  infolding  process  of  gastrulation. 
These  diagrams  aim  to  convey  merely  the  scheme  of  the  process. 
They  are  therefore  simplified  and  emphasize  the  similarities 
of  gastrulation  in  forms  with  widely  varying  amounts  of  yolk, 
rather  than  the  details  of  the  process  in  any  one  form.  With 
this  general  groundwork  we  may  now  profitably  return  to  the 
blastula  stage  and  consider  in  somewhat  more  detail  the  process 
of  gastrulation  as  it  occurs  in  birds. 

Gastrulation  in  Birds. — We  have  already  estabhshed  the 
blastula  as  a  disc  of  cells  lying  on  the  yolk  but  separated  from  it 
centrally  by  a  flattened  blastoccele  or  segmentation  cavity. 
The  peripheral  part  of  the  blastoderm  where  the  marginal  cells 
lie  unseparated  from  the  yolk  has  been  termed  the  zone  of 
junction  (Fig.  7,  Z^).  This  part  of  the  blastoderm  is  also  called 
the  area  opaca  because  in  preparations  made  by  removing  the 
blastoderm  from  the  yolk  surface,  yolk  adheres  to  it  and  renders 
it  more  opaque.  This  opacity  is  especially  apparent  when  a 
preparation  is  viewed  under  the  microscope  by  transmitted 
light.  The  central  area  of  the  blastoderm,  because  it  is  sepa- 
rated from  the  yolk  by  the  segmentation  cavity,  does  not  bring 
a  mass  of  adherent  yolk  with  it  when  the  blastoderm  is  removed. 
It  is  for  this  reason  translucent  and  is  called  the  area  pellucida. 
The  area  opaca  later  becomes  differentiated  so  that  three  more 
or  less  distinct  zones  may  be  distinguished:  (i)  a  peripheral 
zone  known  as  the  margin  of  overgrowth  where  rapid  prolifera- 
tion has  pushed  the  cells  out  over  the  yolk  without  their  becom- 
ing adherent  to  it;  (2)  an  intermediate  zone  known  as  the  zone 
of  junction  in  which  the  deep-lying  cells  do  not  have  complete 
cell  boundaries  but  constitute  a  syncytium  blending  without 
definite  boundary  into  the  superficial  layer  of  white  yolk  and 
adhering  to  it  by  means  of  penetrating  strands  of  cytoplasm; 
(3)  an  inner  zone  known  as  the  germ  wall  made  up  of  cells 
derived  from  the  inner  border  of  the  zone  of  junction  which  have 
acquired  definite  boundaries  and  become  more  or  less  free  from 
the  yolk.  The  cells  of  the  germ  wall  usually  contain  numerous 
small  yolk  granules  which  were  enmeshed  in  their  cytoplasm 
when  they  were,  as  cells  of  the  zone  of  junction,  unseparated 
from  the  yolk  (Fig.  7,  By  E).  The  inner  margin  of  the  germ 
wall  marks  the  transition  from  area  opaca  to  area  pellucida. 


ESTABLISHMENT   OF   THE   ENTODERM 


The  changes  in  the  blastula  which  indicate  the  approach  of 
gastrulation  are,  first,  a  thinning  of  the  blastoderm  at  its  caudal 
margin  and,  second,  freeing  of  the  blastoderm  from  the  yolk 


in  the  same  region  (Fig.  7,  Z)).  The  separation  of  the  blasto- 
derm from  the  yolk  is  evidenced  in  surface  views  by  a  crescentic 
gap  in  the  posterior  quadrant  of  the  zone  of  junction  (Fig.  y,  A). 


26  EARLY  EMBRYOLOGY  OF  THE  CHICK 

This  region  where  the  blastoderm  is  thin  and  free  from  the  yolk 
marks  the  position  of  the  blastopore. 

Gastrulation  begins  with  the  undertucking  of  the  cells  at  the 
free  margin  of  the  blastoderm.  Figure  7,  B,  is  a  diagrammatic 
surface  view  of  the  blastoderm  represented  as  a  transparent 
object.  The  position  and  the  extent  of  the  invaginated  ento- 
derm seen  through  the  overlying  ectoderm  are  indicated  by 
the  cross  hatched  area.  The  appearance  of  the  blastopore 
locates  the  caudal  region  of  the  future  embryo  and  permits  the 
definition  of  its  longitudinal  axis.  This  axis  is  indicated  by  the 
line  b-b  on  Figure  7,  B.  A  diagram  of  a  section  cut  in  the 
longitudinal  axis  and  passing  through  the  blastopore  of  an 
embryo  of  this  stage  is  shown  in  Figure  7,  E.  The  invaginated 
cells  which  constitute  the  entoderm  form  a  layer  extending 
cephalad  from  the  thickened  lip  of  the  blastopore.  The  yolk 
forms  the  floor  of  the  gastroccele.  Figure  7,  C,  is  a  diagrammatic 
surface-view  of  a  later  stage  in  the  same  process.  The  extent 
of  the  entoderm  is  marked  by  cross-hatching  as  in  the  diagram 
of  the  previous  stage.  The  undertucking  of  the  cells  at  the 
blastopore  has  ceased  by  this  time,  and  as  indicated  in  Figure 
7,  C.  by  the  black  area,  and  in  Figure  7,  F,  by  the  solid  mass  of 
cells  seen  in  section,  the  blastopore  has  become  closed. 

During  the  entire  time  that  the  process  of  gastrulation  has 
been  in  progress  there  has  been  constant  cell  proliferation  going 
on  in  the  blastoderm  as  a  whole.  The  growth  of  the  blastoderm 
has  been  evidenced  especially  by  increase  in  its  surface  extent 
which  has  resulted  in  a  general  spreading  of  its  peripheral  mar- 
gins over  the  yolk.  This  extension  has  taken  place  uniformly 
at  all  parts  of  the  margin  except  in  the  posterior  quadrant  where 
the  blastopore  is  located.  Here  the  cells  proliferated,  instead 
of  spreading  out  over  the  yolk  have  turned  in  at  the  lip  of  the 
blastopore  to  form  the  invaginated  entoderm.  This  particular 
part  of  the  margin  of  the  blastoderm,  having  contributed  the 
cells  formed  in  its  growth  to  the  entoderm  which  grows  back 
toward  the  center  of  the  blastoderm,  takes  no  part  in  the 
general  peripheral  expansion.  As  a  result  the  blastopore  region 
is,  as  it  were,  left  behind  and  the  rapidly  extending  margin  of 
the  blastoderm  on  either  side  sweeps  around  and  encloses  it. 
The  blastopore  at  the  time  of  its  closure  thus  comes  to  lie 
within  the  recompleted  circle  of  the  germ  wall  (Fig.  7,  C). 


CHAPTER  V 

THE   FORMATION    OF   THE    PRIMITIVE    STREAK   AND 
THE  ESTABLISHMENT  OF  THE  MESODERM 

The  location  and  appearance  of  the  primitive  streak; 
the  origin  of  the  primitive  streak  by-  concrescence 

OF  THE  blastopore;  THE  FORMATION  OF  THE  MESODERM. 

The  Location  and  Appearance  of  the   Primitive  Streak. 

The  stages  of  development  described  in  the  preceding  chapters 
take  place  before  the  egg  is  laid.  The  first  conspicuous  struc- 
tural feature  to  make  its  appearance  in  the  embryo  after  the 
laying  of  the  egg  is  the  primitive  streak.  In  eggs  that  have  been 
incubated  about  i6^hours  the  primitive  streak  is  well  developed 

cephalic  end 


Hensen's  node 
area  pellucida 

area  opaca 


primitive  pit 


primitive  groove 


primitive  ridge 


Fig.  8. 


■Dorsal  view  (  X  14)  of  entire  chick  embryo  in  the  primitive  streak  stage 
(about  16  hours  of  incubation). 


as  a  linear  groove  flanked  on  either  side  by  ridge-like  thickenings, 
extending  from  the  inner  margin  of  the  area  opaca  to  approxi- 
mately the  center  of  the  blastoderm  (Fig.  8).  The  primitive 
streak  Hes  in  the  longitudinal  axis  of  the  future  embryo.  The 
end  adjacent  to  the  area  opaca  is  its  posterior  (caudal)  end, 
the  opposite  extremity  is  its  anterior  (cephalic)  end.     The  ce- 


27 


28  EARLY  EMBRYOLOGY   OF   THE   CHICK 

phalic  end  of  the  primitive  groove  is  deepened  and  often  some- 
what expanded  to  form  a  depression  known  as  the  primitive  pit. 
Directly  anterior  to  the  primitive  pit  the  right  and  left  primitive 
folds  merge  with  each  other  in  the  mid-line  to  form  a  small 
rounded  elevation  called  Hensen's  node.  Hensen's  node  is  of 
importance  as  a  landmark  rather  than  because  it  gives  rise  to 
any  particular  structure. 

As  early  as  the  beginning  of  gastrulation  the  shape  of  the 
blastoderm  responds  to  local  inequality  in  the  rate  of  growth. 
One  of  the  early  manifestations  of  differential  growth  is  the 
more  rapid  extension  of  the  embryo  cephalad  than  either 
laterad  or  caudad.  This  results  in  a  definite  elongation  in 
the  antero-posterior  axis  by  the  time  the  primitive  streak  is 
established  (Fig.  8). 

The  Origin  of  the  Primitive  Streak  by  Concrescence  of  the 
Blastopore. — The  significance  of  the  primitive  streak  has  been 
the  subject  of  much  controversy.  The  divergences  of  opinion 
have  been  due  chiefly  to  incomplete  knowledge  of  the  stages 
of  development  passed  through  prior  to  the  laying  of  the  egg. 
Our  present  knowledge  of  these  early  stages  is,  however,  suffi- 
cient to  furnish  the  basis  of  an  interpretation  of  the  primitive 
streak  which  is  now  widely  accepted.  This  interpretation  is 
outlined  below  without  reference  to  other,  opposed  views. 

The  primitive  streak  is  to  be  regarded  as  a  scar-like  thicken- 
ing arising  from  the  fusion  of  the  edges  of  the  anterior  lip  of  the 
blastopore.  To  understand  the  origin  of  the  longitudinally 
placed  primitive  streak  from  the  marginally  located,  crescentic 
blastopore  it  is  necessary  to  follow  carefully  the  growth  proc- 
esses taking  place  during  the  closure  of  the  blastopore. 

We  have  already  seen  how  the  ingrowth  of  entoderm  from 
the  anterior  lip  of  the  blastopore,  caused  the  blastopore  to  lag 
behind  the  other  parts  of  the  margin  of  the  blastoderm  in  the 
process  of  radial  extension  over  the  yolk  surface.  During  this 
process  the  blastopore  is  compressed  from  either  side  toward 
the  mid-line  by  the  rapidly  extending  margins  of  the  blastoderm 
adjacent  to  it  and  is  eventually  encompassed  by  them  (see 
Chap.  IV  and  Fig.  7).  Because  of  the  insweeping,  converging 
tendency  of  the  growth  which  first  causes  the  blastopore  to  be 
laterally  compressed  and  finally  causes  its  margins  to  grow 
together  the  process  has  been  termed  concrescence. 


FORMATION   OF   THE   PRIMITIVE    STREAK 


29 


A  schematic  interpretation  of  four  steps  in  the  concrescrnce 
of  the  margins  of  the  blastopore  is  given  in  the  diagrams  of 
Figure  9.  The  blastoderm  shown  in  surface- view  plan  in 
Figure  9,  ^,  is  approximately  at  the  same  stage  of  gastrulation  as 
that  indicated  in  Figure  7,  B.  To  avoid  complicating  the 
diagarm,  the  entoderm  has  not  been  shown  in  Figure  9.  Num- 
bers have  been  placed  along  the  lip  of  the  blastopore  to  facilitate 


marginal  notch 


Fig.  9. — Schematic  diagrams  to  illustrate  the  concrescence  theory  of  the  origin 
of  the  primitive  streak.     {After  Lillie.)     For  explanation  see  text. 


following  the  changes  in  position  undergone  by  the  points  to 
which  they  are  affixed.  As  the  margins  of  the  blastoderm 
adjacent  to  the  blastopore  grow,  they  tend  to  converge  in  the 
direction  indicated  by  the  arrows  in  Figure  g,  B.  The  anterior 
lip  of  the  blastopore  is  folded  on  itself  by  this  converging  growth. 
The  middle  point  of  the  lip,  i,  comes  to  lie  within  the  margin  of 
the  blastoerdm,  and  points,  2,  2,  which  formerly  lay  laterally  are 


30  EARLY   EMBRYOLOGY   OF   THE   CHICK 

brought  into  apposition  in  the  mid  Hne.  Figures  C,  and  D, 
show  how,  by  the  continuation  of  the  same  converging  growth, 
the  edges  of  the  blastopore  are  folded  together  into  a  line  of 
fusion  at  right  angles  to  the  Original  marginal  position  of  the 
blastopore.  At  the  completion  of  concrescence,  the  germ  wall  of 
the  blastoderm  has  coalesced  posterior  to  the  blastopore  leaving 
the  line  along  which  the  blastopore  lips  have  fused  within  the 
area  pellucida.  The  non-committal  term  primitive  streak  was 
given  to  this  structure  before  its  origin  by  fusion  of  the  lips  of 
the  blastopore  was  suspected. 

The  Formation  of  the  Mesodenn. — In  its  early  condition  the 
primitive  streak  is  a  scarcely  recognizable  thickening  of  the 
blastoderm  marking  the  line  of  fusion  of  the  hps  of  the  blasto- 
pore. The  well  defined  groove  with  thickened  ridges  on  either 
side,  seen  in  chicks  of  15  to  1 6  hours  incubation,  is  a  later  devel- 
opment. A  new  process,  the  formation  of  the  mesoderm,  is 
taking  place  at  this  region  and  the  change  in  the  configuration 
of  the  primitive  streak  is  its  outward  manifestation.  It  will 
be  recalled  that  the  lip  of  the  blastopore  is  in  all  forms  a  region 
of  rapid  cell  proHferation.  It  is  a  region  from  which  we  can 
trace  the  addition  of  cells  to  the  differentiated  germ  layers,  but 
it  is  itself  indifferent.  Ectoderm  and  entoderm  both  merge 
into  this  indifferent  area  at  the  lip  of  the  blastopore.  It  is 
impossible  to  fix,  except  arbitrarily,  where  ectoderm  begins  and 
entoderm  ends.  Later  when  the  mesoderm  appears,  we  can 
trace  the  origin  of  its  cells  directly  or  indirectly  to  the  same 
area  of  indifferent,  rapidly  prohferating  cells.  It  is  therefore 
wholly  in  Hne  with  the  embryology  of  other  forms  to  find  the 
mesoderm  of  the  chick  arising  at  the  fused  lips  of  the  blastopore. 

The  manner  in  which  the  mesoderm  arises  can  be  understood 
only  by  the  study  of  sections  or  diagrams  of  sections.  Figure 
10,  A,  represents  schematically  the  conditions  which  would  be 
seen  in  a  section  cut  in  the  hne  h-h  across  the  marginal  notch 
of  an  embryo  of  the  stage  depicted  in  Figure  9,  B.  The  mar- 
gins of  the  blastopore  at  the  point  where  this  section  is  located 
have  been  folded  so  they  lie  in  close  proximity  to  each  other. 
A  Httle  later  they  would  be  fused  as  shown  in  Figure  10,  B. 
At  the  region  of  fusion,  that  is  to  say  at  the  primitive  streak, 
the  entoderm  and  ectoderm  merge  in  a  mass  of  rapidly  dividing 
cells  (Fig.  13,  Z>).     A  section  across  the  primitive  streak  at  a 


FORMATION    OF   THE   PRIMITIVE    STREAK 


31 


somewhat  later  stage  (Fig.  10,  C)  shows  cells  extending  to 
either  side  of  the  undifferentiated  cell  mass,  between  the  ecto- 
derm and  the  entoderm.  These  cells  are  the  primordium  of 
the  third  of  the  germ  layers,  the»mesoderm.  The  outgrowth  of 
the  mesoderm  and  the  median  depression  in  the  primitive  streak 
appear  synchronously.  This  median  depression  in  the  primi- 
tive streak  is  the  primitive  groove.  It  is  not  unhkely  that  the 
formation  of  the  primitive  groove  is  due  to  cell  rearrangement 


lips  of  blastopore 

A 


y^jj  ^^-'"■^  I  ^*^~  entodenn 


primitive  g;ut 


yolk 


primitive  gut 


primitive  groove 


Fig.  10. — Diagrams  showing  schematically  the  relations  of  the  germ  layers 
during  the  formation  of  the  primitive  streak  by  concrescence  of  the  margins  of 
the  blastopore.  A,  hypothetical  section  of  blastoderm  at  the  stage  represented 
in  Fig.  9,  B.  The  plane  of  the  section  is  indicated  by  the  line  h-h  Fig.  9,  B. 
B,  hypothetical  section  of  blastoderm  at  the  stage  represented  in  Fig.  9,  D. 
The  plane  of  the  section  is  indicated  by  the  line  d-d.  Fig.  9,  D.  C,  schematic 
transverse  section  through  the  primitive  streak  at  the  stage  represented  in 
Fig.  8. 


in  this  region  entailed  by  the  rapid  outgrowth  of  the  cells  con- 
stituting the  mesoderm.     (See  arrows  in  Figure  lo,  C.) 

With  the  formation  of  the  mesoderm  the  chick  has  estab- 
lished the  three  germ  layers  characteristic  of  all  vertebrate 
embryos.  The  importance  of  these  layers  lies  in  the  uniformity 
of  their  origin  and  history.  From  them  the  development  of  all 
the  organ  systems  may  be  traced.     The  ectoderm  gives  rise  to 


32  EARLY  EMBRYOLOGY   OF   THE   CHICK 

the  outer  epithelial  covering  of  the  body  and  its  derivatives 
(feathers,  claws,  skin  glands,  etc.) ,  the  nervous  system,  and  the 
sense  organs.  The  entoderm  gives  rise  to  the  epithelial  lining 
of  the  digestive  tube  and  of  the  respiratory  organs  and  the 
epitheHum  of  their  associated  glands.  The  mesoderm  becomes 
differentiated  to  form  the  fibrous  and  rigid  connective  tissues 
(except  neuroglia)  the  muscle,  the  epithelial  lining  of  the  body 
cavities,  the  organs  of  the  circulatory  system,  the*  blood,  the 
lymphatic  organs  and  the  major  part  of  the  urino-genital 
system  of  the  adult. 


CHAPTER  VI 

FROM  THE  PRIMITIVE  STREAK  STAGE  TO  THE 
APPEARANCE  OF  THE  SOMITES 

The  primitive  streak  as  a  center  of  growth;  the  growth 
of   the   entoderm   and   the   establishment   of   the 

PRIMITIVE  gut;  the  GROWTH  AND  DIFFERENTIATION  OF  THE 
MESODERM;  THE  FORMATION  OF  THE  NOTOCHORD;  THE 
FORMATION  OF  THE  NEURAL  PLATE;  THE  DIFFERENTIATION 
OF  THE  EMBRYONAL  AREA. 

The  Primitive  Streak  as  a  Center  of  Growth. — The  impor- 
tance of  the  primitive  streak  embryologically,  is  due  chiefly  to  the 
way  it  is  involved  in  the  estabHshment  of  the  germ  layers. 
Representing  as  it  does  the  fused  lips  of  the  blastopore  it  marks 
the  location  of  entoderm  invagination.  The  mesoderm  also 
arises  at  the  primitive  streak  region.  The  general  appearance 
and  the  location  of  the  primitive  streak  are  both  well  shown  in 
embryos  of  i6  hours  of  incubation  (Fig.  8).  In  embryos  which 
have  been  incubated  i8  hours  (Fig.  ii)  the  primitive  streak  is 
still  the  most  conspicuous  feature.  Structurally  it  is  little 
changed  from  the  conditions  seen  in  1 6-hour  chicks,  but  it  appears 
to  be  somewhat  more  caudally  located.  In  21  to  2  2 -hour  em- 
bryos (Fig.  14)  the  primitive  streak  lies  still  farther  caudal  in 
the  blastoderm.  Its  change  in  position  is  relative  rather  than 
actual.  The  apparent  change  in  the  position  of  the  primitive 
streak  is  due  to  the  fact  that  growth  is  taking  place  more  rapidly 
cephalic  to  it  than  caudal  to  it.  This  tendency  is  in  evidence 
throughout  the  early  growth  of  the  embryo.  The  cephalic 
region  is  precocious  in  development.  As  development  pro- 
gresses we  shall  find  the  primitive  streak  occupying  a  constantly 
more  posterior  position  in  the  body  and  being  more  and  more 
overshadowed  by  the  greater  growth  of  the  structures  lying 
cephalic  to  it. 

The  structure  of  the  primitive  streak  region  is  best  shown 
by  transverse  sections.  In  the  sections  diagrammed  in  Figure 
3  .      33 


34 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


13,  a  different  conventional  scheme  of  representation  has  been 
employed  to  indicate  each  of  the  germ  layers.  The  ectoderm  is 
vertically  hatched,  the  cells  of  the  mesoderm  are  represented 
by  heavy  angular  dots  when  they  are  isolated  or  by  solid  black 
lines  when  they  lie  arranged  in  the  form  of  compact  layers, 
and  the  entoderm  is  represented  by  fine  stippHng  backed  by  a 
single  line.  This  same  conventional  representation  of  the 
different  germ  layers  is  observed  in  all  diagrams  of  sections  in 


anterior  border 
of  mesoderm 


neural  plate. 


embryonal  area  ■ 


area  pellucida- 
area  opaca 


-r: 


notochord 
-Hensen's  node 


'primitive  streak 


caudal  end 
Pig.  II. — Dorsal  view  (  X  14)  of  entire  chick  embryo  of  18  hours  incubation. 


order  to  facilitate  following  the  way  in  which  the  organ  systems 
of  the  embryo  are  constructed  from  the  germ  layers.  Details 
of  cell  structure  are  for  the  most  part  omitted  with  the  expecta- 
tion that  the  student  will  acquire  a  knowledge  of  them  in  his 
own  study  of  sections.  The  plane  in  which  each  of  the  sections 
diagrammed  passes  through  the  embryo  is  indicated  by  a  line 
drawn  on  a  small  outline  sketch  of  an  embryo  of  corresponding 
stage.  For  interpretation  these  outline  sketches  should  be 
compared  with  actual  specimens  or  detailed  drawings  of  entire 
embryos  of  the  same  stage  of  development. 

In  embryos  of  the  stage  under  consideration  the  relationship 
of  the  germ  layers  at  the  primitive  streak  still  indicates  their  man- 
ner of  derivation  (Fig.  13,  C  and  D).     The  ectoderm  and  the 


PRIMITIVE    STREAK   TO   SOMITE   FORMATION  35 

entoderm  are  continuous  with  each  other  without  any  demarca- 
tion. The  mesoderm  arises  from  the  primitive  streak  where 
ectoderm  and  entoderm  merge  and  grows  laterad  on  both  sides  of 
the  primitive  streak  extending  into  the  space  between  ectoderm 
and  entoderm.  The  mass  of  cells  in  the  floor  of  the  primitive 
groove  is  to  be  regarded  as  constituting  an  undifferentiated  area 
from  which  new  cells  are  being  proUferated  rapidly  and  are 
emigrating  to  become  components  of  one  or  another  of  the  germ 
layers. 

To  those  who  have  studied  the  embryology  of  more  primitive 
vertebrates,  particularly  the  Amphibia,  the  fact  that  the  lips 
of  the  blastopore  constitute  centers  of  growth  from  which  cells 
are  pushed  forth  to  take  part  in  the  formation  of  the  differenti- 
ated germ  layers  will  already  be  famiHar.  The  fact  that  the 
blastopore  of  the  chick  has  suffered  a  change  in  position  due  to 
concrescence,  and  has  in  the  same  process  become  closed  by 
fusion  of  its  Ups  must  not  be  allowed  to  obscure  its  homologies. 
In  attempting  to  bring  the  relationships  of  the  germ  layers  in 
the  chick  into  Hne  with  the  relationships  of  the  germ  layers  in 
embryos  having  less  yolk,  it  will  be  of  great  assistance  to  picture 
a  chick  lifted  off  the  yolk  and  the  lateral  margins  of  the  blasto- 
derm pulled  together  ventrally;  or,  the  method  of  comparison 
may  be  reversed  if  one  imagines  the  embryo  of  a  form  having 
less  yolk,  such  as  an  amphibian,  to  be  split  open  along  the  mid- 
ventral  line  and  spread  out  on  the  surface  of  a  sphere  as  a  chick 
lies  on  the  yolk. 

In  Figure  13,  D,  a  small  region  at  the  primitive  streak  has 
been  drawn  at  higher  magnification  to  show  the  characteristic 
cellular  structure  of  the  undifferentiated  region  in  the  floor  of 
the  primitive  groove  and  of  the  various  layers  merging  at  this 
place.  The  cells  of  the  ectoderm  are  much  more  closely  packed 
together  and  more  sharply  delimited  than  those  of  the  other 
germ  layers.  Where  the  ectoderm  is  thickened  in  the  primitive 
ridge  region,  it  is  several  cell  layers  thick  (stratified).  (Fig.  13, 
D.)  In  regions  lateral  to  the  primitive  ridge  it  gradually  be- 
comes thinner  until  it  consists  of  but  a  single  cell  layer  (Fig.  13, 
E).  The  rapid  extension  that  the  mesoderm  is  at  this  time 
undergoing  is  indicated  by  the  loose  arrangement  and  sprawling 
appearance  of  its  cells.  Their  irregular  cytoplasmic  processes, 
make  them  look  much  Hke  amoebae  fixed  during  locomotion. 


36  EARLY  EMBRYOLOGY   OF   THE   CHICK 

The  cells  of  the  entoderm  are  neither  as  closely  packed  nor  as 
clearly  defined  as  are  the  ectoderm  cells.  Nevertheless,  in 
contrast  to  the  condition  of  the  mesoderm  at  this  stage,  the 
entoderm  cells  form  a  definite,  unbroken  layer. 

The  Growth  of  the  Entoderm  and  the  Establishment  of 
the  Primitive  Gut. — Sections  of  embryos  of  this  stage  show 
how  the  entoderm  has  spread  out  and  become  organized  into  a 
coherent  layer  of  cells  merging  peripherally  with  the  inner  mar- 
gin of  the  germ  wall  and  overlapping  it  to  a  certain  extent 
(Fig.  13,  C,  E,  F).  The  cavity  between  the  yolk  and  the  ento- 
derm which  has  been  called  the  gastrocoele  is  now  termed  the 
primitive  gut.  The  yolk  floor  of  the  primitive  gut  does  not 
show  in  sections  prepared  by  the  usual  methods.  The  reasons 
for  this  are  to  be  found  in  the  relations  of  the  embryo  to  the 
yolk  before  it  is  removed  for  sectioning.  In  the  entire  central 
region  of  the  blastoderm  the  yolk  is  separated  from  the  ento- 
derm by  the  cavity  of  the  primitive  gut.  When  the  embryo  is 
removed  from  the  yolk  sphere  the  yolk  floor  of  the  primitive 
gut,  not  being  adherent  to  the  blastoderm,  is  left  behind.  In 
contrast  the  peripheral  part  of  the  blastoderm  lies  closely  ap- 
pHed  to  the  yolk.  Some  yolk  adheres  to  this  part  of  the  blasto- 
derm when  it  is  removed.  This  adherent  yolk  is  shown  in  the 
section  diagrams  of  Figure  13.  Its  presence  clearly  indicates 
why  this  region  (area  opaca)  appears  less  translucent  in  surface 
views  of  entire  embryos. 

In  embryos  of  18  hours  the  primitive  gut  is  a  cavity  with 
a  flat  roof  of  entoderm  and  a  floor  of  yolk.  Peripherally  it  is 
bounded  on  all  sides  by  the  germ  wall  (Fig.  13,  C,  F).  The 
merging  of  the  cells  of  the  entoderm  with  the  yolk  mass  is 
shown  in  the  small  area  of  the  germ  wall  drawn  to  a  high  mag- 
nification in  Figure  13,  £.  In  the  germ  wall  cell  boundaries 
are  incomplete  and  very  difiicult  to  distinguish  but  nuclei  can 
be  made  out  surrounded  by  more  or  less  definite  areas  of  cyto- 
plasm. This  cytoplasm  contains  numerous  yolk  granules  in 
various  stages  of  absorption.  It  will  be  recalled  that  the  nuclei 
of  the  germ  wall  arise  by  division  from  the  nuclei  of  cells  lying 
at  the  margins  of  the  expanding  blastoderm.  They  appear  to 
be  concerned  in  breaking  up  the  yolk  in  advance  of  the  ento- 
derm as  it  is  spreading  about  the  yolk  sphere. 

About  the  twenty-second  hour  of  incubation  indications  can 


PRIMITIVE    STREAK   TO    SOMITE   FORMATION  37 

be  seen  of  a  local  differentiation  of  that  region  of  the  primitive 
gut  which  underHes  the  anterior  part  of  the  embryo.  By  focus- 
ing through  the  ectoderm  in  the  anterior  region  of  a  whole- 
mount  of  this  age  a  pocket  of  entoderm  can  be  seen  (Fig.  14). 
This  entodermal  pocket  is  the  first  part  of  the  gut  to  acquire  a 
floor,  other  than  the  yolk  floor,  and  is  called  from  its  anterior 
position  the  fore-gut.  Consideration  of  the  fore-gut  except  to 
note  the  location  of  its  first  appearance  can  advantageously  be 
deferred  because  its  origin  and  relationships  are  more  readily 
appreciated  from  the  study  of  somewhat  older  embryos. 

The  Growth  and  Differentiation  of  the  Mesoderm. — The 
mesoderm  which  arises  from  either  side  of  the  primitive  streak 
spreads  rapidly  laterad  and  at  the  same  time  each  lateral 
wing  of  the  mesoderm  swings  cephalad.  Figure  12  shows 
schematically  the  extension  of  the  mesoderm  during  the  latter 
part  of  the  first  day  of  incubation.  The  diagonal  hatch- 
ing represents  the  mesoderm  seen  through  the  transparent 
ectoderm.  The  principal  landmarks  of  the  embryos  are 
sketchily  represented. 

It  will  be  noticed  that  the  manner  in  which  the  mesoderm 
spreads  out  leaves  a  mesoderm-free  area  in  the  anterior  portion 
of  the  blastoderm.  This  region  is  known  as  the  proamnion. 
The  name  might  carry  the  inference  that  this  area  is  the  primor- 
dium  of  the  amnion,  a  structure  which  first  appears  near  this 
region  somewhat  later  in  development.  Such  is  not  the  fact. 
The  term  proamnion  was  applied  to  this  region  before  its  true 
significance  was  understood.  It  is  not  the  precourser  of  the 
amnion.  In  dorsal  views  of  entire  embryos  the  proamnion  is 
readily  located  by  reason  of  its  lesser  density.  The  proamnion 
is  bounded  anteriorly  by  the  area  opaca,  posteriorly  in  the  mid- 
line by  the  thickened  anterior  part  of  the  embryo,  and  poste- 
riorly on  either  side  by  the  anterior  bordero  f  the  mesoderm 
(Fig.  12).  The  importance  of  the  proamnion  lies  chiefly  in  the 
indication  it  gives  of  the  progress  of  mesoderm  extension.  The 
rapid  growth  that  the  mesoderm  of  the  anterior  region  is  under- 
going at  this  stage  is  clearly  indicated  by  the  diminution  in 
area  of  the  proamnion  in  embryos  of  22  hours  as  compared  with 
embryos  of  18  hours  (Fig.  12). 

Sections  passing  through  the  primitive  streak  of  embryos  of 
this  stage  show  the  pair  of  loosely  aggregated  masses  of  meso- 


38 


EARLY   EMBRYOLOGY    OF    THE    CHICK 


derm  extending  to  either  side  between  the  ectoderm  and  ento- 
derm. As  would  be  expected  from  the  method  of  origin,  little 
mesoderm  appears  in  the  mid-line  except  posterior  to  the  primi- 
tive streak.  Immediately  to  either  side  of  the  mid-line  the 
mesoderm  is  markedly  thicker  than  it  is  farther  laterad  (Fig. 
IS,  B).     In  whole-mounts  the  positions  of  the  regional  thicken- 


^.J^  primitive 
streak 


peUucida. 


CHICK  OF  ABOUT  14  HOURS. 


anterior  horn    of 
mesoderm 


...^n'i^+^. 


]2      CHICK  OF  ABOUT  18  HOURS, 
proamnion 


dorsal  mesoderm 


primitive  streak 


V^      CHICK  OF  ABOUT  22  HOURS. 

Pig.  12. — Schematic  diagrams  to  show  the  extension  of  the  mesoderm  during 
the  latter  part  of  the  first  day  of  incubation.  Some  of  the  more  prominent 
structural  features  of  the  embryos  are  drawn  in  lightly  for  orientation  but  the 
ectoderm  is  supposed  to  be  nearly  transparent  allowing  the  mesoderm  to  show 
through.  The  areas  into  which  the  mesoderm  has  grown  are  indicated  by 
diagonal  hatching.  ^^ 

ings  of  the  mesoderm  are  evidenced  by  the  greater  opacity  they 
impart  to  the  embryo  locally  (Fig.  14).  These  thickened  zones 
of  the  mesoderm  are  the  primordia  of  the  dorsal  mesodermic 
plates.     Because  of  the  way  in  which  they  are  later  divided  into 


PRIMITIVE    STREAK   TO    SOMITE    FORMATION 


39 


■^^m^^^ 


prumtive  gut 


nucleus 
cell  in  mitosis  ^  ^^^  „f  ^^j^  granules  - 

entoderm  indifferent  cells 


I   J     High  power  thru  primitive  streak  at  region  (a) 
on  section  C. 


"C^       High  power  thru  edge  of  germ  wall 
at  region  (b)  on  section  C. 


Hensen'snode  primitive 

neural  plate  |  .primitive  pit  ridge 

'j)rimitive  groove  ' 


extent  of  primitive  gut  and  of  area  pellucida 


Pig.  13. — Sections  of  iS-hoxir  chick.  The  location  of  each  section  is  indicated 
by  a  line  drawn  on  a  small  outline  sketch  of  an  entire  embryo  of  corresponding 
age.  The  letters  affixed  to  the  lines  indicating  the  location  of  the  sections 
correspond  with  the  letters  designating  the  section  diagrams.  Each  germ 
layer  is  represented  by  a  different  conventional  scheme:  ectoderm  by  vertical 
hatching;  entoderm  by  fine  stippling  backed  by  a  single  line;  and  the  cells  of 
the  mesoderm  which  at  this  stage  do  not  form  a  coherent  layer,  by  heavy  angular 
dots. 

A,  diagram  of  transverse  section  through  notochord;  B,  diagram  of  transverse 
section  through  primitive  pit;  C,  diagram  of  transverse  section  through  primitive 
streak;  D,  drawing  showing  cellular  structure  in  primitive  streak  region;  E, 
drawing  showing  cellular  structure  at  inner  margin  of  germ  wall;  F,  diagram 
of  median  longitudinal  section  passing  through  notochord  and  primitive  streak. 


40  EARLY  EMBRYOLOGY   OF   THE   CHICK 

metamerically  arranged  cell  masses  or  somites  they  are  fre- 
quently designated  as  the  segmental  zones  of  the  mesoderm. 
The  segmental  zones  are  in  early  stages  most  clearly  marked 
somewhat  cephalic  to  Hensen's  node,  where  the  first  somites 
will  appear.  As  they  extend  caudad  on  either  side  of  the 
primitive  streak  they  gradually  become  less  and  less  definite. 

The  sheet-like  layers  of  mesoderm  which  are  characteristic 
of  the  mid-body  region  do  not  extend  to  the  anterior  part  of 
the  embryo.  The  mesoderm  of  the  future  head  region  is 
derived  from  mesoderm  cells  which  invade  the  head  from  the 
more  definitely  organized  layers  of  mesoderm  lying  posterior  to 
it.  The  cephaHc  mesoderm  for  this  reason  never  shows  the 
regional  differentiations  and  the  organization  into  definite  layers 
which  later  appear  in  the  mesoderm  of  the  mid-body  region. 

The  Formation  of  theNotochord. — The  notochord  arises  in  the 
chick  as  a  median  out-growth  from  the  rapidly  proliferating, 
undifferentiated  cells  at  the  cephalic  end  of  the  primitive  streak 
(Fig.  is,F).  The  way  in  which  the  notochord  grows  cephalad 
from  the  anterior  end  of  the  primitive  streak,  just  as  in  other 
vertebrate  embryos  it  arises  from  the  region  of  the  anterior  lip  of 
the  blastopore,  is  one  of  the  points  which  confirms  the  identifica- 
tion of  the  primitive  streak  of  the  chick  as  the  closed  blastopore. 

Largely  because  of  the  way  in  which  the  notochord  arises  in 
Amphioxus,  a  primitive  vertebrate  of  doubtful  relationships,  it 
has  usually  been  considered  of  entodermal  origin.  In  Amphibia 
and  in  birds  it  arises  not  from  any  definite  germ  layer  but  from 
the  undifferentiated  growth  center  about  the  blastopore  which 
is  giving  rise  to  both  entoderm  and  mesoderm.  Even  in  Am- 
phioxus the  notochord  arises  at  the  same  time  and  in  the  same 
manner  as  the  mesoderm.  In  its  later  differentiation  the  noto- 
chord resembles  mesodermal  derivatives  more  closely  than 
entodermal.  The  common  origin  of  notochord  and  mesoderm, 
and  the  unmistakably  mesodermal  characteristics  of  the  fully 
developed  notochord  should  be  emphasized  rather  than  the 
early  association  of  the  notochordal  primordium  with  the 
entoderm  and  its  doubtful  origin  therefrom.  For  these  reasons 
the  notochord  is  in  this  book  treated  as  a  mesodermal  structure. 

In  entire  embryos  of  i8  to  22  hours  (Figs.  11  and  14)  the 
notochord  can  be  seen  in  the  mid-line  extending  cephalad  from 
Hensen's  node.     Hensen's  node  is  at  once  the  posterior  limit 


PRIMITIVE    STREAK   TO    SOMITE   FORMATION 


41 


of  the  notochord  and  the  anterior  end  of  the  primitive  streak. 
The  notochord  and  the  primitive  streak  together  clearly  mark 
the  mid-line  of  the  embryo  and  estabUsh  definitely  the  longitu- 
dinal axis  of  the  developing  body.  In  sections  (Fig.  13,  ^,  F) 
the  notochord  is  not  at  this  early  stage  sharply  differentiated 
from  the  loosely  arranged  mesoderm  cells  adjacent  to  it.  In 
later  stages,  however,  the  cells  composing  it  become  aggregated 
to  form  a  characteristic  rod-shaped  structure,  circular  in  cross 
section  and  with  clearly  defined  boundaries  (Fig.  52,  C). 

The  Formation  of  the  Neural  Plate. — In  surface  views  of  en- 
tire chicks  of  about  18  hours  (Fig.  11)  areas  of  greater  density 


cephalic  end 


ectoderm  of  head 


border  of  fore-gut 


margin  of  anterior 
intestinal  portal 


notochord 


primitive  streak 


area  pellucida 


area  opaca 


caudal  end 
Fig.  14. — Dorsal  view  (  X  14)  of  entire  chick  embryo  of  about  21  hours  incubation. 


may  be  made  out  on  either  side  of  the  notochord.  These  areas 
extend  somewhat  anterior  to  the  cephaUc  end  of  the  notochord 
where  they  appear  to  blend  with  each  other  in  the  mid-hne. 
Sections  of  this  region  (Fig.  13,  A)  show  that  the  greater 
density  seen  in  whole-mounts  is  due  to  thickening  of  the  ecto- 
derm. Rapid  cell  proHferation  has  resulted  in  the  ectoderm 
in  the  middle  region  becoming  several  cells  in  thickness.     This 


42  EARLY   EMBRYOLOGY   OF   THE   CHICK 

thickened  area  is  known  as  the  neural  (medullary)  plate. 
Laterally  the  thickened  ectoderm  of  the  neural  plate  blends 
without  abrupt  transition  into  the  thinner  ectoderm  of  the 
general  blastodermic  surface.  Anteriorly  the  neural  plate  is 
more  clearly  marked  than  it  is  posteriorly.  At  the  level  of 
Hensen's  node  the  neural  plate  diverges  into  two  elongated  areas 
of  thickening  one  on  either  side  of  the  primitive  streak. 

In  embryos  of  21  or  22  hours  (Fig.  14)  the  neural  plate 
becomes  longitudinally  folded  to  estabHsh  a  trough  known  as 
the  neural  groove.  The  bottom  of  the  neural  groove  lies  in 
the  mid-dorsal  line.  Flanking  the  neural  groove  on  each  side 
is  a  longitudinal  ridge-like  elevation  involving  the  lateral  por- 
tion of  the  neural  plate.  These  two  elevations  which  bound 
the  neural  groove  laterally  are  known  as  the  neural  folds.  The 
folding  of  the  originally  fiat  neural  plate  to  form  a  gutter, 
flanked  on  either  side  by  parallel  ridges,  is  an  expression  of  the 
same  extremely  rapid  cell  proUferation  which  first  manifested 
itself  in  the  local  thickening  of  the  ectoderm  to  form  the  neural 
plate.  The  formation  of  the  neural  plate  and  its  subsequent 
folding  to  form  the  neural  groove  are  the  first  indications  of  the 
differentiation  of  the  central  nervous  system. 

The  Differentiation  of  the  Embryonal  Area.^Due  to  the 
thickening  of  the  ectoderm  to  form  the  neural  plate  and  also 
to  the  thickening  of  the  dorsal  zones  of  the  mesoderm,  the  part 
of  the  blastoderm  immediately  surrounding  the  primitive  streak 
and  notochord  has  become  noticeably  more  dense  than  that 
in  the  peripheral  portion  of  the  area  pellucida.  Because  it  is 
the  region  in  which  the  embryo  itself  is  developed  this  denser 
region  is  known  as  the  embryonal  area.  Although  the  embry- 
onal area  is  at  this  early  stage  directly  continuous  with  the 
peripheral  part  of  the  blastoderm  without  any  definite  Une  of 
demarcation,  they  later  become  folded  off  from  each  other. 
The  peripheral  portion  of  the  blastoderm  is  then  spoken  of  as 
extra-embryonic  because  it  gives  rise  to  structures  which  are 
not  built  into  the  body  of  the  embryo,  although  they  play  a 
vital  part  in  its  nutrition  and  protection  during  development. 

The  anterior  region  of  the  embryonal  area  is  thickened  and 
protrudes  above  the  general  surface  of  the  surrounding  blasto- 
derm as  a  rounded  elevation.  This  prominence  marks  the 
region  in  which  the  head  of  the  embryo  will  develop  (Fig.  14). 


PRIMITIVE    STREAK   TO    SOMITE   FORMATION  43 

The  crescentic  fold  which  bounds  it  is  termed  the  head  fold 
and  is  the  first  definite  boundary  of  the  body  of  the  embryo. 
Throughout  the  course  of  development  we  shall  find  the  head 
region  farther  advanced  in  differentiation  than  other  parts  of 
the  body.  This  is  a  repetition  of  race  history  in  the  develop- 
ment of  the  individual,  for  phylogenetically  the  head  is  the 
oldest  and  most  highly  differentiated  region  of  the  body.  It  is 
one  of  many  manifestations  of  the  law  of  recapitulation,  in 
conformity  with  which  the  individual  in  its  development  rap- 
idly repeats  the  main  steps  in  the  development  of  the  race  to 
which  it  belongs. 


CHAPTER  VII 

THE  STRUCTURE  OF  TWENTY-FOUR  HOUR  CHICKS 

The  formation  of  the  head;  the  formation  of  the  neural 
groove;  the  regional  divisions  of  the  mesoderm;  the 
ccelom,  the  pericardial  region;  the  area  vasculosa. 

The  Formation  of  the  Head. — In  embryos  of  21  to  22  hours 
the  anterior  part  of  the  embryonal  area  is  thickened  and  ele- 
vated above  the  level  of  the  surrounding  blastoderm,  with  a 
well  defined  crescentic  fold  marking  its  anterior  boundary. 
Between  21  and  24  hours  this  region  has  undergone  rapid 
growth  (Fig.  15).  Its  elevation  above  the  blastoderm  is  much 
more  marked  and  it  has  grown  anteriorly  so  it  overhangs  the 
proamnion  region.  The  crescentic  fold  which  formerly  marked 
its  anterior  boundary  appears  to  have  undercut  the  anterior 
part  of  the  embryo  and  separated  it  from  the  blastoderm.  The 
changes  in  relationships  are  due,  however,  not  so  much  to  a 
posterior  movement  of  the  fold  as  to  the  anterior  growth  of  the 
embryo  itself.  This  anterior  region  which  projects,  free  from 
the  blastoderm,  may  now  properly  be  termed  the  head  of  the 
embryo.  The  space  formed  between  the  head  and  the  blasto- 
derm is  called  the  subcephalic  pocket  (Fig.  17,  E). 

In  the  mid-Une  the  notochord  can  be  seen  through  the  over- 
lying ectoderm.  It  is  larger  posteriorly  near  its  point  of  origin 
than  it  is  anteriorly.  Nevertheless  it  can  be  readily  traced  into 
the  cephaUc  region  where  it  will  be  seen  to  terminate  somewhat 
short  of  the  anterior  end  of  the  head  (Fig.  15). 

The  Formation  of  the  Neural  Groove. — The  neural  plate  in 
chicks  of  18  hours  was  seen  as  a  flat,  thickened  area  of  the  ecto- 
derm. In  embryos  of  21  to  22  hours  a  longitudinal  folding  had 
involved  it  establishing  the  neural  groove  in  the  mid-dorsal 
line  flanked  on  either  side  by  the  neural  folds.  At  24  hours  of 
incubation  the  folding  of  the  neural  plate  is  much  more  clearly 
marked.  In  a  dorsal  view  of  the  entire  embryo  (Fig.  15)  the 
neural  folds  appear  as  a  pair  of  dark  bands.     The  folding  which 

44 


STRUCTURE    OF   TWENTY-FOUR   HOUR   CHICKS 


45 


establishes  the  neural  groove  takes  place  first  in  the  cephalic 
region  of  the  embryo.  At  its  cephalic  end  the  neural  groove 
is  therefore  deeper  and  the  neural  folds  are  correspondingly 
more  prominent  than  they  are  caudally.  The  folding  has  not, 
at  this  stage,  been  carried  much  beyond  the  cephalic  half  of 
the  embryo.  Consequently  as  the  neural  folds  are  followed 
caudad  they  diverge  slightly  from  each  other,  and  become  less 
and  less  distinct. 


ectoderm  of  head 


border  of  fore-gut 


subcephalic  pocket 


Hensen's  node 


.unsegmented 
Jy'^^'.'-'i'i^f^yC'^'^     mesoderm 

l^&piW^W^'V       primitive 
i-<':-.A-iV=:s,..':35C*«-  ■  -,treak 


border  of  mesoderm 


blood  island 


area  vasculosa 


Pig.  15. — Dorsal  view  (  X  14)  of  entire  chick  embryo  having  4  pairs  of  meso- 
dermic  somites  (about  24  hours  incubation). 

Study  of  transverse  sections  of  an  embryo  of  this  stage  affords 
a  clearer  interpretation  of  the  conditions  in  neural  groove  for- 
mation than  the  study  of  entire  embryos.  A  section  passing 
through  the  head  region  (Fig.  ly,  A)  shows  the  neural  plate 
folded  so  it  forms  a  nearly  complete  tube.  Dorsally  the  mar- 
gins of  the  neural  folds  of  either  side  have  approached  each 
other  and  lie  almost  in  contact.  The  formation  of  the  neural 
folds  takes  place  first  in  about  the  center  of  the  head  region, 
and  progresses  thence  cephalad  and  caudad.  By  following 
caudad  the  sections  of  a  transverse  series,  the  margins  of  the 


46 


EARLY   EMBRYOLOGY    OF    THE    CHICK 


neural  folds  will  be  seen  less  and  less  closely  approximated  to 
each  other. 

The  Establishment  of  the  Fore-gut. — In  the  outgrowth  of  the 
head,  the  entoderm  as  well  as  the  ectoderm  has  been  involved. 
As  a  result  the  entoderm  forms  a  pocket  within  the  ectoderm, 
much  like  a  small  glove  finger  within  a  larger.  This  entodermic 
pocket,  or  fore-gut,  is  the  first  part  of  the  digestive  tract  to  ac- 
quire a  definite  cellular  floor.  That  part  of  the  gut  caudal  to  the 
fore-gut  where  the  yolk  still  constitutes  the  only  floor,  is  termed 
the  mid-gut.  The  opening  from  the  mid-gut  into  the  fore-gut 
is  called  the  anterior  intestinal  portal  (fovea  cardiaca) . 


margin  of  anterior 
horn  of  mesoderm 

pourior  margin  of     '^ 
subcephalic  pocket 


margin  of  fore-gut  -Js 


margin  of  Aiterior 

intestinal  portal 

(entoderm) 

notochord 


11  r : 


margin  of  area  opaca 


ectoderm  of  head 


" —  mesenchyme 


■     „      border  of  mesoderm 

— —    pericardial  region 
of  coelom 

~ —  thickened   splanchnic 
mesoderm 


neural  fold 


Pig.  i6. — Ventral  view  (  X  37)  of  cephalic  region  of  chick  embryo  having  5  pairs 
of  somites  (about  25-26  hours  of  incubation). 

The  topography  of  the  fore-gut  region  at  this  stage  can  be 
made  out  very  well  by  studying  the  ventral  aspect  of  entire 
embryos.  The  margin  of  the  anterior  intestinal  portal  appears 
as  a  well  defined  crescentic  Une  (Fig.  i6).  The  lateral  boun- 
daries of  the  fore-gut  can  be  seen  to  join  the  caudally  directed 
tips  of  the  crescentic  margin  of  the  portal.  Considerably 
cephalic  to  the  intestinal  portal  an  irregularly  recurved  hne  can 
be  made  out.  On  either  side  it  appears  to  merge  with  the  ecto- 
derm of  the  head.  This  Hne  marks  the  extent  to  which  the 
head  is  free  from  the  blastoderm.  It  is  due  to  the  fold  at  the 
bottom  of  the  subcephalic  pocket  where  the  ectoderm  of  the 
under  surface  of  the  head  is  continuous  with  the  ectoderm  of  the 
blastoderm.  Comparison  of  Figure  16  with  the  sagittal  section 
diagrammed  in  Figure  17,  -E,  will  aid  in  making  clear  the  rela- 


STRUCTURE    OF   TWENTY-FOUR   HOUR   CHICKS  47 

tionships  of  fore-gut  to  the  head.  From  the  sagittal  section  it 
will  also  be  apparent  why  the  margins  of  the  intestinal  portal 
and  of  the  subcephalic  pocket  appear  as  dark  lines  in  the  whole- 
mount.  In  viewing  an  entire  embryo  under  the  microscope  by 
transmitted  light  one  depends  largely  on  differences  in  density 
for  locating  deep-lying  structures.  When  a  layer  is  folded  so 
the  light  must  pass  through  it  edgewise,  the  fold  stands  out  as  a 
dark  hne  by  reason  of  the  greater  thickness  it  presents. 

The  Regional  Divisions  of  the  Mesoderm. — The  first  con- 
spicuous metamerically  arranged  structures  to  appear  in  the 
chick  are  the  mesodermic  somites.  The  somites  arise  by  divi- 
sion of  the  mesoderm  of  the  dorsal  or  segmental  zone  to  form 
block-Hke  cell  masses.  In  the  embryo  shown  in  Figure  15  three 
pairs  of  somites  are  completely  delimited  and  a  fourth  pair  can 
be  made  out  which  is  not  as  yet  completely  cut  off  from  the 
dorsal  mesoderm  posterior  to  it. 

The  regular  addition  of  somites  as  embryos  increase  in  age 
makes  the  number  of  somites  the  most  reliable  criterion  of  the 
stage  of  development.  Chicks  which  have  been  incubated  for 
a  given  number  of  hours  show  wide  variation  in  the  degree  of 
development  attained;  chicks  of  a  given  number  of  somites 
vary  but  little  among  themselves.   ' 

Cross  sections  passing  through  the  rnid-body  region  show  the 
formation  of  the  somites  and  the  beginning  of  other  changes  in 
the  mesoderm  (Fig.  17,  C,  cf.  also  Fig.  28,  E).  Following  the 
mesoderm  from  the  mid-line  toward  either  side  three  regions  or 
zones  can  be  made  out:  (i)  the  dorsal  mesoderm  which  at  this 
level  has  been  organized  into  somites,  (2)  the  intermediate 
mesoderm,  a  thin  plate  of  cells  connecting  the  dorsal  and  lateral 
mesoderm  and  (3)  the  lateral  mesoderm  which  is  distinguished 
from  the  intermediate  by  being  split  into  two  layers  with  a  space 
between  them. 

The  somites  are  compact  cell  masses  lying  immediately 
lateral  to  the  neural  folds  The  cells  composing  them  have  a 
fairly  definite  radial  arrangement  about  a  central  cavity  which 
is  very  minute  or  wanting  altogether  when  the  somites  are  first 
formed  but  which  later  becomes  enlarged  (Fig.  38).  Cephalic 
and  caudal  to  the  region  in  which  somites  have  been  formed  the 
dorsal  mesoderm  is  differentiated  from  the  rest  of  the  mesoderm 
simply  by  its  greater  thickness  and  compactness. 


48 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


In  24-hour  embryos  the  intermediate  mesoderm  shows  very 
little  differentiation.  In  the  chick  it  never  becomes  segmentally 
divided  as  does  the  dorsal  mesoderm.  The  fact  that  it  is 
potentially  segmental  in  character  is  indicated,  however,  by 
the  way  in  which  it  later  gives  rise  to  segmentally  arranged 


proamnion 
region 


primitive 
ridge 


Fig.  17. — Diagrams  of  sections  of  24-hour  chick.  The  sections  are  located 
on  an  outline  sketch  of  the  entire  embryo.  The  conventional  representation  of 
the  germ  layers  is  the  same  as  that  employed  in  Fig.  13  except  that  here  where 
its  cells  have  become  aggregated  to  form  definite  layers  the  mesoderm  is  repre- 
sented by  heavy  solid  black  lines. 

nephric  tubules.  Because  of  the  part  it  plays  in  the  establish- 
ment of  the  excretory  system  the  intermediate  mesoderm  is 
frequently  called  the  nephrotomic  plate. 


STRUCTURE    OF   TWENTY-FOUR   HOUR   CHICKS  49 

In  the  chick  the  lateral  mesoderm  like  the  intermediate 
mesoderm,  shows  no  segmental  division.  In  24-hour  embryos 
(Fig.  17,  C)  it  is  clearly  differentiated  from  the  intermediate 
mesoderm  by  being  split  horizontally  into  two  layers  with  a 
space  between  them.  The  layer  of  lateral  mesoderm  lying 
next  to  the  ectoderm  is  termed  the  somatic  mesoderm,  the  layer 
next  to  the  entoderm  is  termed  the  splanchnic  mesoderm,  and 
the  cavity  between  somatic  and  splanchnic  mesoderm  is  the 
coelom.  Because  in  development  the  somatic  mesoderm  and 
ectoderm  are  closely  associated  and  undergo  many  foldings  in 
common,  it -is  convenient  to  designate  the  two  layers  together 
by  the  single  term  somatopleure.  Similarly  the  splanchnic 
mesoderm  and  the  entoderm  together  are  designated  as  the 
splanchnopleure. 

The  Coelom. — The  coelom,  like  the  cell  layers  of  the  blasto- 
derm, extends  over  the  yolk  peripherally  beyond  the  embryonal 
area  (Fig.  17,  C).  Later  in  development  foldings  mark  off  the 
embryonic  from  the  extra-embryonic  portion  of  the  germ  layers. 
This  same  folding  process  divides  the  coelom  into  intra-em- 
bryonic  and  extra-embryonic  regions.  In  the  24-hour  chick, 
however,  embryonic  and  extra-embryonic  coelom  have  not  been 
separated. 

It  is  evident  from  the  manner  in  which  the  coelomic  chambers 
arise  in  the  lateral  mesoderm  that  the  coelom  of  the  embryo  con- 
sists of  a  pair  of  bilaterally  symmetrical  chambers.  It  is  not 
until  later  in  development  that  the  right  and  left  coelomic 
chambers  become  confluent  ventrally  to  form  an  unpaired 
body  cavity  such  as  is  found  in  adult  vertebrates. 

The  Pericardial  Region. — In  the  region  of  the  anterior  intes- 
tinal portal  the  coelomic  chambers  on  either  side  show  very 
marked  local  enlargements.  Later  in  development  these 
dilated  regions  are  extended  mesiad  and  break  through  into 
each  other  ventral  to  the  fore-gut  to  form  the  pericardial  cavity. 
In  their  early  condition  these  enlarged  regions  of  the  coelomic 
chambers  are  usually  called  amnio-cardiac  vesicles.  With  their 
later  fate  in  mind  we  may  avoid  multiplication  of  terms  and 
speak  of  them  from  their  first  appearance  as  constituting  the 
pericardial  region  of  the  coelom. 

The  relationships  of  the  pericardial  region  of  the  coelom  in 
embryos  of  24  hours  can  be  most  readily  grasped  from  a  study 


50  EARLY   EMBRYOLOGY   OF   THE   CHICK 

of  transverse  sections.  Figure  17,  B,  shows  the  great  dilation 
of  the  coelom  on  either  side  of  the  anterior  intestinal  portal  as 
compared  with  its  condition  farther,  caudad  (Fig.  17,  C). 
Where  the  splanchnic  mesoderm  lies  closely  applied  to  the 
entoderm  at  the  lateral  margins  of  the  portal  it  is  noticeably 
thickened.  It  is  from  these  areas  of  thickened  splanchnic 
mesoderm  that  the  paired  primordia  of  the  heart  will  later 
arise. 

In  entire  embryos  of  this  age  the  thickened  splanchnic 
mesoderm  can  be  made  out  as  a  dark  band  lying  close  against 
the  crescentic  entodermal  border  of  the  anterior  intestinal 
portal  (Fig,  16).  If  the  preparation  is  favorably  stained  the 
boundaries  of  the  pericardial  regions  of  the  coelom  can  be  traced 
(see  Fig.  16).  Following  mesiad  from  the  easily  located  thick- 
ened areas,  the  mesodermic  borders  can  be  seen  to  extend  from 
either  side  parallel  to  the  entodermic  margins  of  the  portal 
nearly  to  the  mid-line.  They  then  turn  cephalad.  When  they 
encounter  the  ectodermal  fold  which  constitutes  the  posterior 
boundary  of  the  subcephalic  pocket  they  swing  laterad  parallel 
with  it  and  can  be  traced  outside  the  embryonic  region  where 
they  constitute  the  cephalic  borders  of  the  anterior  horns  of 
the  mesoderm  (see  also  Fig.  27,  A). 

The  portion  of  the  coelom,  the  borders  of  which  we  have  just 
located  between  the  subcephalic  pocket  and  the  anterior  in- 
testinal portal,  is  an  important  landmark  from  another  stand- 
point than  the  part  it  is  destined  to  play  in  the  formation  of  the 
pericardial  region.  It  is  the  most  cephalic  part  of  the  coelom. 
There  is  no  coelom  in  the  head.  In  the  head  region  the  meso- 
derm is  not  aggregated  into  definite  masses  or  coherent  cell 
layers.  The  mesodermic  structures  of  the  head  are  derived 
from  cells  which  migrate  into  the  cephahc  region  from  the  meso- 
derm lying  farther  caudally.  These  migrating  cells  are  termed 
mesenchymal  cells  in  distinction  to  the  more  definitely  aggre- 
gated cell  layers  of  the  mesoderm.  By  careful  focusing  on  the 
whole-mount  the  mesenchyme  of  the  head  can  be  seen  as  an 
indefinite  mass  lying  between  the  superficial  ectoderm  and  the 
entoderm  of  the  fore-gut.  The  distribution  of  the  mesenchymal 
cells  and  the  characteristic  irregularity  of  shape  correlated 
with  their  active  amoeboid  movement  may  be  readily  made  out 
from  sections  (Fig.  17,  ^4). 


STRUCTURE   OF   TWENTY-FOUR  HOUR   CHICKS  5 1 

The  Area  Vascvilosa. — In  a  24-hour  chick  the  boundary  be- 
tween area  opaca  and  area  pellucida  has  the  same  appearance 
and  significance  as  in  chicks  of  18  to  20  hours.  There  is,  how- 
ever, a  very  marked  difference  between  the  proximal  portion 
of  the  area  opaca  adjacent  to  the  area  pellucida  and  the  more 
distal  portions  of  the  area  opaca.  The  proximal  region  is  much 
darker  and  has  a  somewhat  mottled  appearance  (Fig.  1 5) .  The 
greater  density  of  this  region  is  due  to  its  invasion  by  mesoderm 
which  makes  it  thicker  and  therefore  more  opaque  in  transmitted 
light  (Fig.  17,  D).  The  boundary  between  the  inner  and  outer 
zones  of  the  area  opaca  is  established  by  the  extent  to  which 
the  mesoderm  has  grown  peripherally.  The  distal  zone  is 
called  the  area  opaca  vitellina  because  the  yolk  alone  underlies 
it.  The  proximal  zone  into  which  mesoderm  has  grown  is 
known  as  the  area  opaca  vasculosa,  because  it  is  from  the  meso- 
derm in  this  region  that  the  yolk-sac  blood  vessels  arise.  The 
mottled  appearance  of  this  region  is  due  to  the  aggregation  of 
mesoderm  into  cell  clusters,  or  blood  islands,  which  mark  the 
initial  step  in  the  formation  of  blood  vessels  and  blood  corpus- 
cles. Later  in  development  the  formation  of  blood  islands  and 
vessels  extends  in  toward  the  body  of  the  embryo  from  its 
place  of  earhest  appearance  in  the  area  opaca  and  involves  the 
mesoderm  of  the  area  pellucida.  The  histological  nature  of 
the  blood  islands  will  be  taken  up  in  connection  with  later 
stages  where  their  development  is  more  advanced. 


CHAPTER  VIII 

THE  CHANGES  BETWEEN  TWENTY-FOUR  AND  THIRTY- 
THREE  HOURS  OF  INCUBATION 

The  closure  of  the  neural  tube;  the  differentiation 
of  the  brain  region;  the  anterior  neuropore;  the 
sinus  rhomboidalis;  the  fate  of  the  primitive  streak; 
the  lengthening  of  the  fore-gut;  the  appearance 
of  the  heart  and  omphalomesenteric  veins;  organ- 
IZATION IN  THE   AREA  VASCULOSA. 

In  dealing  with  developmental  processes  the  selection  of 
stages  for  detailed  consideration  is  more  or  less  arbitrary  and 
largely  determined  by  the  phenomena  one  seeks  to  emphasize. 
There  is  no  stage  of  development  which  does  not  show  some- 
thing of  interest.  It  is  impossible  in  brief  compass  to  take  up 
at  length  more  than  a  few  stages.  Nevertheless  it  is  important 
not  to  lose  the  continuity  of  the  processes  involved.  By  calling 
attention  to  some  of  the  more  important  intervening  changes, 
this  brief  chapter  aims  to  bridge  the  gap  between  the  24-hour 
stage  and  the  33-hour  stages  of  the  chick  both  of  which  are 
taken  up  in  some  detail. 

The  Closure  of  the  Neural  Tube. — In  comparison  with  24- 
hour  chicks,  entire  embryos  of  27  to  28  hours  of  incubation 
(Fig.  18)  show  marked  advances  in  the  development  of  the 
cephalic  region.  The  head  has  elongated  rapidly  and  now  pro- 
jects free  from  the  blastoderm  for  a  considerable  distance,  with 
a  corresponding  increase  in  the  depth  of  the  subcephalic  pocket 
and  in  the  length  of  the  fore-gut. 

In  24-hour  chicks  the  anterior  part  of  the  neural  plate  is 
already  folded  to  form  the  neural  groove.  Although  the  neural 
folds  are  at  that  stage  beginning  to  converge  mid-dorsally  the  ^ 
groove  nevertheless  remains  open  throughout  its  length  (Fig. 
ly.  A,  B,  C).  By  27  hours  the  neural  folds  in  the  cephalic 
region  meet  in  the  mid-dorsal  line  and  their  edges  become  fused. 

The  fusion  which  occurs  is  really  a  double  one.  Careful 
following  of  Figures  26,  A  to  £,  will  aid  greatly  in  understanding 

52 


CHANGES  BETWEEN  24  AND  ^^    HOURS 


53 


the  process.  Each  neural  fold  consists  of  a  mesial  component 
which  is  thickened  neural  plate  ectoderm,  and  a  lateral  com- 
ponent which  is  unmodified  superficial  ectoderm  (Fig.  26,  A), 
When  the  neural  folds  meet  in  the  mid-dorsal  line  (Fig.  26,  -B,  C) 
the  mesial,  neural  plate  components  of  the  two  folds  fuse  with 
each  other,  and  the  outer  layers  of  unmodified  ectoderm  also 
become  fused  (Fig.  26,  D).  Thus  in  the  same  process  the 
neural  groove  becomes  closed  to  form  the  neural  tube  and  the 


proamnion  prosencephalon 

anterior  / 

neuropore 


border  of  fore-gut 


subcephalic  pocket 


mesenchyme 


omphalo- 
mesenteric vein 


blood  island 


border  ot  .....  .^. -y  -.»    . 

inesodenn. '      v^^^v^'^5?iT-;>  '*•. 


rhomboidalis 
Hensen's  node 


.■.-^'^'&f.^"'::<::   ■  ■*  extra-embryonic 
^-  vascular  plexus 


Fig.  18. — Dorsal  view  (  X  14)  of  entire  chick  embryo  having  8  pairs  of  somites 
(about  27-28  hours  incubation). 


superficial  ectoderm  closes  over  the  place  formerly  occupied  by 
the  open  neural  groove.  Shortly  after  this  double  fusion  the 
neural  tube  and  the  superficial  ectoderm  become  somewhat 
separated  from  each  other  leaving  no  hint  of  their  former  con- 
tinuity (Fig.  26,  E). 

The  Differentiation  of  the  Brain  Region. — By  27  hours  of 
incubation  the  anterior  part  of  the  neural  tube  is  markedly 
enlarged  as  compared  with  the  posterior  part.     Its  thickened 


54 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


walls  and  dilated  lumen  mark  the  region  which  will  develop 
into  the  brain.  The  undilated  posterior  part  of  the  neural  tube 
gives  rise  to  the  spinal  cord.  Three  divisions,  the  three  primary 
brain  vesicles,  can  be  distinguished  in  the  enlarged  cephahc 
region  of  the  neural  tube  (Fig.  i8).  Occupying  most  of  the 
anterior-part  of  the  head  is  a  conspicuous  dilation  known  from 
its  position  as  the  fore-brain  or  prosencephalon.     Posterior  to 


ectoderm  of  head 


prosencephalon 


optic  vesicle 


ventral  aortic  root 


ventral  aorta 


epi-myocardium 
endocardium 


line  of  endocardi  al 
fusion 


margin  of  anterior 
intestinal  porta! 


anterior  horn  of  mesoderm 


anterior  neuropore 


infundibulum 


cephalic 
mesenchyme 


extra-embryonic 
vascular  plexus 


Fig.  19. — Ventral  view  (  X  45)  of  head  and  heart  region  of  chick  embryo  of  9 
somites  (about  29-30  hours  incubation). 

the  prosencephalon  and  marked  off  from  it  by  a  constriction  is 
the  mid-brain  or  mesencephalon.  Posterior  to  the  mesenceph- 
alon with  only  a  very  slight  constriction  marking  the  boundary 
is  the  hind-brain  or  rhombencephalon.  The  rhombencephalon 
is  continuous  posteriorly  with  the  cord  region  of  the  neural  tube 
without  any  definite  point  of  transition. 

In  somewhat  older  embryos  (Fig.  19)  the  lateral  walls  of  the 
prosencephalon  become  out-pocketed  to  form  a  pair  of  rounded 
dilations   known   as   the   primary   optic   vesicles.     When   the 


CHANGES  BETWEEN  24  AND  33  HOURS  55 

optic  vesicles  are  first  formed  there  is  no  cgnstriction  between 
them  and  the  lateral  walls  of  the  prosencephalon,  and  the 
lumen  of  each  optic  vesicle  communicates  mesially  with  the 
lumen  of  the  prosencephalon  without  any  definite  hne  of 
demarcation. 

The  relation  of  the  notochord  to  the  divisions  of  the  brain  is  of 
importance  in  later  developmental  processes.  The  notochord 
extends  anteriorly  as  far  as  a  depression  in  the  floor  of  the 
prosencephalon  known  as  the  infundibulum  (Fig.  19).  There- 
fore, the  rhombencephalon,  mesencephalon,  and  that  part  of  the 
prosencephalon  posterior  to  the  infundibulum  he  immediately 
dorsal  to  the  notochord  (are  epichordal)  while  the  infundibular 
region  and  the  parts  of  the  prosencephalon  cephalic  to  it  project 
anterior  to  the  notochord  (are  pre-chordal) . 

The  Anterior  Neuropore. — The  closure  of  the  neural  folds 
takes  place  first  near  the  anterior  end  of  the  neural  groove  and 
progresses  thence  both  cephalad  and  caudad.  At  the  extreme 
anterior  end  of  the  brain  region  closure  is  delayed.  As  a  result 
the  prosencephalon  remains  for  sometime  in  communication 
with  the  outside  through  an  opening  called  the  anterior  neuro- 
pore. The  anterior  neuropore  is  still  open  in  chicks  of  2  7  hours 
(Fig.  18).  In  embryos  of  33  hours  the  neuropore  appears  much 
narrowed  (Fig.  21).  A  little  later  it  becomes  closed  but  leaves 
for  some  time  a  scar-like  fissure  in*  the  anterior  wall  of  the 
prosencephalon  (Fig.  23).  The  anterior  neuropore  does  not 
give  rise  to  any  definite  brain  structure.  It  is  important  simply 
as  a  landmark  in  brain  topography.  Long  after  it  has  disap- 
peared as  a  definite  opening  the  scar  left  by  its  closure  serves  to 
mark  the  point  originally  most  anterior  in  the  developing  brain. 

TheSinusRhomboidalis. — The  rhombencephaUc  region  of  the 
brain  merges  caudally  without  any  definite  line  of  demarcation 
into  the  region  of  the  neural  tube  destined  to  become  the 
spinal  cord.  The  neural  tube  as  far  caudally  as  somite  forma- 
tion has  progressed  is  completely  closed  and  of  nearly  uniform 
diameter.  Caudal  to  the  most  posterior  somites  the  neural 
groove  is  still  open  and  the  neural  folds  diverge  to  either  side  of 
Hensen's  node  (Fig.  18).  In  their  later  growth  caudad  the 
neural  folds  converge  toward  the  mid-line  and  form  the  lateral 
boundaries  of  an  unclosed  region  at  the  posterior  extremity  of 
the  neural  tube  known  because  of  its  shape  as  the  sinus  rhom- 


56  EARLY   EMBRYOLOGY    OF    THE    CHICK 

boidalis  (Fig.  21).  Hensen's  node  and  the  primitive  pit  lie  in 
the  floor  of  this  as  yet  unclosed  region  of  the  neural  groove  and 
subsequently  are  enclosed  within  it  when  the  neural  folds  here 
finally  fuse  to  complete  the  neural  tube. 

This  process  in  the  chick  is  homologous  with  the  enclosure  of 
the  blastopore  by  the  neural  folds  in  lower  vertebrates.  In 
forms  where  the  blastopore  does  not  become  closed  until  after 
it  is  surrounded  by  the  neural  folds,  it  for  a  time  constitutes  an 
opening  from  the  neural  canal  into  the  primitive  gut  known  as 
the  neurenteric  canal  or  posterior  neuropore.  In  the  chick  the 
early  closure  of  the  blastopore  precludes  the  estabHshment  of  an 
open  neurenteric  canal  but  the  primitive  pit  represents  its 
homologue. 

The  Fate  of  the  Primitive  Streak. — In  embryos  of  about  27 
hours  the  primitive  streak  is  relatively  much  shorter  than  in 
younger  embryos  (Cf.  Figs.  8,  11,  14,  15,  and  18).  This  is 
due  partly  to  its  being  overshadowed  by  the  rapid  growth  of 
structures  lying  cephalic  to  it,  and  partly  to  actual  decrease 
in  the  length  of  the  primitive  streak  itself.  The  cells  in  the 
primitive  stieak  region  would  appear  to  be  contributed  to 
surrounding  structures.  Whatever  the  exact  fate  of  its  cells 
may  be,  the  primitive  streak  becomes  less  and  less  a  conspicuous 
feature  in  the  developing  embryo.  By  the  time  the  caudal  end 
of  the  body  is  delimited,  the  primitive  streak  as  a  definitely 
organized  structure  has  disappeared  altogether  (Cf.  Figs.  18, 
21,  29,  34). 

The  Formation  of  Addifional  Somites. — The  division  of  the 
dorsal  mesoderm  to  form  somites  begins  to  be  apparent  in 
embryos  of  about  22  hours.  By  the  end  of  the  first  day  three 
or  four  pairs  of  somites  have  been  cut  off  (Fig.  15).  As  develop- 
ment progresses  new  somites  are  added  caudal  to  those  fiist 
formed.  In  embryos  which  have  been  incubated  about  27 
hours  eight  pairs  of  somites  have  been  established  (Fig.  18). 

It  was  formerly  beHeved  that  some  new  somites  were  formed 
anterior  to  the  first  pair.  The  experiments  of  Patterson  would 
seem  to  indicate  quite  definitely  that  the  first  pair  of  completely 
formed  somites  remains  the  most  anterior  and  that  all  the  new 
somites  are  added  posterior  to  them.  The  experiments  referred 
to  were  carried  out  on  eggs  which  had  been  incubated  up  to  the 
time  of  the  formation  of  the  first  somite.     With  thorough 


CHANGES  BETWEEN  24  AND  33  HOURS         $7 

aseptic  precautions  the  eggs  were  opened  and  the  first  somite 
marked,  in  some  cases  by  injury  with  an  "electric  needle" 
in  other  cases  by  the  insertion  of  a  minute  glass  pin.  Following 
the  operation  the  shell  was  closed  by  sealing  over  the  opening  a 
piece  of  egg  shell  of  appropriate  size.  After  being  again  in- 
cubated for  varying  lengths  of  time  the  eggs  were  reopened.  In 
all  cases  the  injured  first  somite  was  still  the  most  anterior 
complete  somite.  All  the  new  somites  except  the  incomplete 
''head  somite"  had  appeared  caudal  to  the  first  pair  of  somites 
formed. 

The  Lengthening  of  the  Fore-gut. — Comparison  of  the  rela- 
tions of  the  crescentic  margin  of  the  anterior  intestinal  portal 
in  embryos  between  24  and  30  hours  shows  it  occupying  pro- 
gressively more  caudal  positions  (Fig.  27).  This  change  in  the 
position  of  the  anterior  intestinal  portal  is  the  result  of  two 
distinct  growth  processes.  The  margins  of  either  side  of  the 
portal  are  constantly  converging  toward  the  mid-Une  where  they 
become  fused  with  each  other.  Their  fusion  lengthens  the  fore- 
gut  by  adding  to  its  floor  and  thereby  displaces  the  crescentic 
margin  of  the  portal  caudad.  At  the  same  time  the  struc- 
tures cephalic  to  the  anterior  intestinal  portal  are  elongating 
rapidly  so  that  the  portal  becomes  more  and  more  remote  from 
the  anterior  end  of  the  embryo  with  the  further  lengthening  of 
the  fore-gut. 

As  a  result  of  these  two  processes  the  space  between  the  sub- 
cephalic  pocket  and  the  margin  of  the  anterior  intestinal  portal 
is  also  elongated  (Fig.  27).  This  is  of  importance  in  connection 
with  the  formation  of  the  heart  for  it  is  into  this  enlarging 
space  that  the  pericardial  portions  of  the  coelom  extend  and 
in  it  that  the  heart  comes  to  Ue. 

The  Appearance  of  the  Heart  and  Omphalomesenteric  Veins. 
Although  the  early  steps  in  the  formal  ion  of  the  heart  take 
place  in  embryos  of  this  range,  detailed  consideration  of  them 
has  been  deferred  to  be  taken  up  in  connection  with  later  stages 
when  conditions  in  the  circulatory  system  as  a  whole  are  more 
advanced. 

In  dorsal  views  of  entire  embryos  the  heait  is  largely  con- 
cealed by  the  overlying  rhombencephalon  (Fig.  18)  but  it  may 
readily  be  made  out  by  viewing  the  embryo  from  the  ventral 
surface  (Fig.  19).     At  this  stage  the  heart  is  a  nearly  straight 


58  EARLY   EMBRYOLOGY   OF   THE   CHICK 

tubular  structure  lying  in  the  mid-line  ventral  to  the  fore-gut. 
Its  mid-region  has  noticeably  thickened  walls  and  is  somewhat 
dilated.  Anteriorly  the  heart  is  continuous  with  the  large 
median  vessel,  the  ventral  aorta,  posteriorly  it  is  continuous 
with  the  paired  omphalomesenteric  veins.  The  fork  formed 
by  the  union  of  the  omphalomesenteric  veins  in  the  posterior 
part  of  the  heart  lies  immediately  cephalic  to  the  crescentic 
margin  of  the  anterior  intestinal  portal,  the  veins  lying  within 
the  fold  of  entoderm  which  constitutes  its  margin. 

Organization  in  the  Area  Vasculosa. — The  extra-embryonic 
vascular  area  at  this  stage  is  undergoing  rapid  enlargement 
and  presents  a  netted  appearance  instead  of  being  mottled  as 
in  the  earlier  embryos.  The  peripheral  boundary  of  the  area 
vasculosa  is  definitely  marked  by  a  dark  band,  the  precursor 
of  the  sinus  terminalis  (marginal  sinus) .  Its  netted  appearance 
is  due  to  the  extension  and  anastomosing  of  blood  islands. 
The  formation  of  the  network  is  a  step  in  the  organization  of  a 
plexus  of  blood  vessels  on  the  yolk  surface  which  will  later  be 
the  means  of  absorbing  and  transferring  food  material  to  the 
embryo.  The  afferent  yolk-sac  or  vitelline  circulation  is  estab- 
lished in  the  next  few  hours  of  incubation  when  this  plexus  of 
vessels  developing  on  the  yolk  surface  comes  into  communica- 
tion with  the  omphalomesenteric  veins  already  developing 
within  the  embryo  and  extending  laterad.  The  efferent  vitelUne 
circulation  is  established  somewhat  later  when  the  omphalo* 
mesenteric  arteries  arise  from  the  aorta  of  the  embryo  and 
become  connected  with  the  yolk-sac  plexus.  (Cf.  Figs.  15,  18, 
21). 


CHAPTER  IX 

THE  STRUCTURE  OF  CHICKS  BETWEEN  THIRTY-THREE 
AND  THIRTY-NINE  HOURS  OF  INCUBATION 

The  divisions  of  the  brain  and  their  neuromeric  struc- 
ture; THE  auditory  PITS;  THE  FORMATION  OF  EXTRA-EM- 
BRYONIC BLOOD  vessels;  THE  FORMATION  OF  THE  HEART; 
THE   FORMATION  OF  INTRA-EMBRYONIC  BLOOD  VESSELS. 

Chicks  which  have  been  incubated  from  S3  to  39  hours  are 
in  a  favorable  stage  to  show  some  of  the  fundamental  steps  in 
the  foimation  of  the  central  nervous  system,  and  of  the  circu- 
latoi;y  system.  In  this  chapter,  therefore,  attention  has  been 
concentrated  on  these  two  systems. 

During  this  period  of  incubation  there  are  also  changes  in 
the  fore-gut  region  and  in  the  somites,  and  differentiation  in 
the  intermediate  mesoderm  which  presages  the  formation  of 
the  urinary  organs.  Consideration  of  these  structures  has, 
however,  been  defeired  until  their  development  has  progressed 
somewhat  farther. 

The  Divisions  of  the  Brain  and  Their  Neuromeric  Structure. 
The  metameric  arrangement  of  structures  which  is  so  striking 
a  feature  in  the  body  organization  of  all  vertebrates,  is  masked 
in  the  head  region  of  the  adult  by  superimposed  specializations. 
In  the  brain  of  young  vertebrate  embryos,  however,  the  meta- 
merism is  still  indicated.  Dissections  of  the  neural  plate  of 
chicks  at  the  end  of  the  first  day  of  incubation  show  a  series  of 
eleven  enlargements  marked  off  from  each  other  by  contric- 
tions  (Fig.  20,  A).  Concerning  the  precise  homologies  of  indi- 
vidual enlargements  with  specific  neuromeres  in  other  forms 
there  is  not  complete  agreement.  The  controversies  center 
about  the  question  of  neuromeric  fusions  in  the  anterior  part 
of  the  brain.  For  the  beginning  student  the  fact  that  meta- 
merism is  present  is  to  be  emphasized  rather  than  the  contro- 
versies concerning  the  homologies  of  neuromeres.  With  the 
reservation  that  some  of  the  anterior  enlargements  may  repre- 

59 


6o 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


sent  fusions  of  more  than  one  neuromere,  the  series  of  enlarge- 
ments seen  in  the  brain  region  of  the  chick  may  be  regarded  as 
neuromeric.  For  convenience  in  designation  the  neuromeres 
are  numbered  beginning  at  the  anterior  end. 


anterior  neuropore 


cut  ectoderm 

neural  groove 

Hft  neural  fold 


neuromeric 
enlargement 


line  of  fusion 
neural  folds 


rhombencephalon 


prosencephalon 


mesencephalon 


metencephalon 


myelencephalon 


Pig.  20. — Diagrams  to  show  the  neuromeric  enlargements  in  the  brain  region 
of  the  neural  tube.  (Based  on  figures  by  Hill.) 
A ,  lateral  view  of  neural  plate  from  dissection  of  chick  of  4  somites  (24  hours) ; 
B,  dorsal  view  of  brain  dissected  out  of  7-somite  (26  to  27-hour)  embryo;  C, 
dorsal  view  of  brain  trom  lo-somite  (30-hour)  embryo;  D,  dorsal  view  of  brain 
from  14-somite  (36-hour)  embryo. 

\\  ith  the  closure  of  the  neural  tube  and  the  establishment  of 
the  three  primary  brain  vesicles  we  can  begin  to  trace  the  fate  of 


STRUCTURE    OF    THIRTY-THREE   HOUR   CHICKS 


6l 


the  vaiious  neuromeric  enlargements  in  the  formation  of  the 
brain  regions.  The  three  anterior  neuromeres  form  the  prosen- 
cephalon; neuromeres  four  and  five  are  incorporated  in  the 
mesencephalon;  and  neuromeres  six  to  eleven  in  the  rhom- 


prosencephalon 

proamnion 


anterior  neuropore 

optic  vesicle 


omphalomesenteric  vein 


lateral  m 


sinus  rhomboidalis 


primitive  streak 


Pig.  21. — Dorsal  view  (  x  14)  of  an  entire  chick  embryo  of  12  somites  (about 
33  hours  incubation). 

b^ncephalon  (Fig.  20,  B).  Anteriorly  the  interneuromeric 
constrictions  soon  disappear  except  for  two;  namely,  the  one 
between  the  prosencephalon  and  mesencephalon,  and  the  one 


62 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


between  the  mesencephalon  and  rhombencephalon.  The 
rhombencephalic  neuromeres,  however,  remain  clearly  marked 
for  a  considerable  period. 

By  about  33  hours  of  incubation  the  optic  vesicles  are  estab- 
lished as  paired  lateral  outgrowths  of  the  prosencephalon. 
They  soon  extend  to  occupy  the  full  width  of  the  head  (Fig. 
20,  C  and  Fig.  21).     The  distal  portion  of  each  of  the  vesicles 


>-'5- 


^fir     ***»»»„,„ 


-v.^> 


prosencephalon 


cctodeim 


S' 

^"'m,,^ 

^  optic  vesicle 

infundibulum  -—^ 

'    :!'^' 

-^^m 

L^m 

^^^^ 

mesencephalon 

*' 

^^m^ 

^^_^....r^-^  aortic  arch 

ventral 

-''1 

r^'HrTfWR 

f^f 

J 

. 

if  He             Vi    m3  T 

j 

,- — i*^ notochord 

■> 

■i^JR       y    i  jMI  i 

f  / 

siSm  {  ^^Km 

Ki 

HeHI    <<  '''^^n'ln^ 

/ 

^       **                                  r    f 

region  of  ganglion  V 

VWF  Imv^''^1 

}j 

metencephalon  ^ 

4" 

-^H^^P^ 

'/ 

t      , 

myelencephalon  ^- 

{ 

SQ 

^^^\ 

"  '                        irteriosus 

cephalic  neural  ere  at  — 

region  of  ganglion 

^^T^n-i^Jv*?^  i 

VII    VIII 

t^iUHB  ;AnL#'«HSpid 

■    ' 

■■r 

'AjPjBK-glW  ■      ^  -, 

i 

'WmU^ 

*^    V  >• 

L^^^  S-fll^^ 

- 

I  ^^S  vl^^  I 

vein 

Pig.  22. — Dorsal  view  (  x  45)  of  head  and  heart  region  of  a  chick  embryo  of  17 
somites  (38-39  hours  incubation). 

thus  comes  to  lie  closely  approximated  to  the  superficial  ecto- 
derm, a  relationship  of  importance  in  their  later  development. 
At  first  the  cavities  of  the  optic  vesicles  (opticoeles)  are  broadly 
confluent  with  the  cavity  of  the  prosencephalon  (prosoccele) . 
Somewhat  later  constrictions  appear  which  mark  more  defi- 
nitely the  boundaries  between  the  optic  vesicles  and  the  prosen- 
cephalon (Fig.  20,  D  and  Fig.  22). 

There  arises  also  at  this  stage  a  depression  in  the  floor  of  the 


STRUCTURE    OF    THIRTY-THREE   HOUR    CHICKS 


63 


prosencephalon  known  because  of  its  peculiar  shape  as  the 
infundibulum  (Figs.  23  and  24).  The  infundibular  region  is 
the  site  of  important  changes  later  in  development.  At  this 
stage,  conditions  are  not  sufficiently  a^dvanced  to  warrant  more 
than  calling  attention  to  its  origin  from,  and  relations  to,  the 
prosencephalon,  and  to  the  anterior  end  of  the  notochord  as 
shown  in  the  figures  referred  to. 


prosencephalon 

nfundibulum 


bulbo-conus  arteriosus 
cut  epi-myocardium 

ventricular  region  . 
atrial  region 

-anterior  intestinal  portal 


ventral  aortic  roots 


cut  ectoderm 


dorsal  aortae 


stnus  venosus 


lateral  mesoderm 


cut  splanchnopleure 


Pig.  23. — Diagrammatic  ventral  view  of  dissection  of  a  35-hour  chick  embryo. 
{Modified  from  Prentiss.)  The  splanchnopleure  of  the  yolk-sac  cephalic  to  the 
anterior  intestinal  portal,  the  ectoderm  of  the  ventral  surface  of  the  head,  and 
the  mesoderm  of  the  pericardial  region,  have  been  removed  to  show  the  under- 
lying structures.  Figure  24  should  be  referred  to  for  the  relations  of  the  peri- 
cardial mesoderm. 

In  chicks  of  about  38  hours  indications  of  the  impending 
division  of  the  three  primary  vesicles  to  form  the  five  regions 
characteristic  of  the  adult  brain  are  already  beginning  to  ap- 
pear. In  the  establishment  of  the  five-vesicle  condition  of 
the    brain,    the    prosencephalon    is   subdivided   to  form   the 


64 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


STRUCTURE   OF   THIRTY-THREE  HOUR   CHICKS  65 

telencephalon  and  diencephalon,  the  mesencephalon  remains 
undivided,  and  the  rhombencephalon  divides  to  form  the 
metencephalon  and  myelencephalon. 

The  division  of  the  prosencephalon  into  telencephalon  and 
diencephalon  is  not  completed  until  a  much  later  stage  of 
development,  but  the  median  enlargement  at  this  stage  ex- 
tending anterior  to  the  level  of  the  optic  vesicles  indicates  where 
the  telencephalon  will  be  established  (Fig.  20,  D).  The  optic 
vesicles  and  that  part  of  the  prosencephalon  lying  between  them 
go  into  the  diencephalon. 

The  mesencephalon,  as  stated  above,  undergoes  no  subdivi- 
sion. The  original  mesencephalic  region  of  the  three-vesicle 
brain  gives  rise  to  the  mesencephalon  of  the  adult.  This  region 
of  the  brain  does  not  undergo  any  marked  differentiation  until 
relatively  late  in  development. 

At  this  stage  the  division  of  the  rhombencephalon  is  clearly 
marked  (Fig.  20,  D  and  Fig.  22).  The  two  most  anterior 
neuromeres  of  the  original  rhombencephalon  form  the  meten- 
cephalon and  the  posterior  four  neuromeres  are  incorporated 
in  the  myelencephalon. 

The  Auditory  Pits. — As  is  the  case  with  the  central  nervous 
system,  the  organs  of  special  sense  arise  early  in  development. 
The  appearance  of  the  optic  vesicles  which  later  become  the 
sensory  part  of  the  eyes  has  already  been  noted.  The  first 
indication  of  the  formation  of  the  sensory  part  of  the  ear 
becomes  evident  at  about  35  hours  of  incubation.  At  this  age 
a  pair  of  thickenings  termed  the  auditory  placodes  arise  in  the 
superficial  ectoderm  of  the  head.  They  are  situated  on  the 
dorso-lateral  surface  opposite  the  most  posterior  inter-neuro- 
meric  constriction  of  the  myelencephalon.  By  38  hours  of 
incubation  (Fig.  22)  the  auditory-  placodes  have  become 
depressed  below  the  general  level  of  the  ectoderm  and  form 
the  walls  of  a  pair  of  cavities,  the  auditory  pits.  When  first 
formed  the  walls  of  the  auditory  pits  are  directly  continuous 
with  the  superficial  ectoderm,  and  their  cavities  are  widely  open 
to  the  outside.  In  later  stages  the  openings  into  the  pits 
become  narrowed  and  finally  closed  so  that  the  pits  become 
vesicles  lying  between  the  superficial  ectoderm  and  the  myelen- 
cephalon. As  yet  they  have  no  connection  with  the  central 
nervous  system. 


66  EARLY  EMBRYOLOGY   OF   THE   CHICK 

The   Formation   of   Extra-embryonic   Blood  Vessels. — In 

dealing  with  the  circulation  of  the  chick  we  must  recognize 
at  the  outset  two  distinct  circulatory  arcs  of  which  the  heart  is 
the  common  center.  One  complete  circulatory  arc  is  estab- 
lished entirely  within  the  body  of  the  embryo.  A  second  arc  is 
established  which  has  a  rich  plexus  of  terminal  vessels  located 
in  the  extra-embryonic  membranes  enveloping  the  yolk.  These 
are  the  vitelline  vessels.  The  vitelline  vessels  communicate 
with  the  heart  over  main  vessels  which  traverse  the  embryonic 
body.  The  chief  distribution  of  the  vitelline  circulation  is, 
however,  extra-embryonic.  Later  in  development  there  arises 
a  third  circulatory  arc  involving  another  set  of  extra-embryonic 
vessels  in  the  allantois,  but  with  that  we  have  no  concern  until 
we  take  up  later  stages.  Neither  the  intra-embryonic,  nor  the 
vitelline  circulatory  channels  have  as  yet  been  completed  but 
the  heart  and  many  of  the  main  vessels  have  made  their 
appearance. 

The  formation  of  extra-embryonic  blood  vessels  is  presaged 
by  the  appearance  of  blood  islands  in  the  vascular  area  of 
chicks  toward  the  end  of  the  first  day  of  incubation  (see  Chapter 
Vll).  Figure  25  shows  the  differentiation  of  blood  islands  to 
form  primitive  blood  corpuscles  and  blood  vessels.  At  their 
first  appearance  the  blood  islands  are  irregular  clusters  of  meso- 
derm cells  lying  in  intimate  contact  with  the  yolk-sac  entoderm 
(Fig.  25,  A).  When  the  lateral  mesoderm  becomes  split 
forming  the  somatic  and  splanchnic  layers  with  the  coelom 
between,  the  blood  islands  lie  in  the  splanchnic  mesoderm  ad- 
jacent to  the  entoderm.  In  embryos  of  3  to  5  somites  fluid 
filled  spaces  begin  to  appear  in  the  blood  islands  with  the  result 
that  in  each  blood  island  the  peripheral  cells  are  separated  from 
the  central  ones  (Fig.  25,  -B).  As  the  fluid  accumulates  and  the 
spaces  expand  the  peripheral  cells  become  flattened  and^ushed 
outward,  but  they  remain  adherent  to  each  other  and  com- 
pletely enclose  the  central  cells.  At  this  stage  the  single  layer 
of  peripheral  cells  may  be  regarded  as  constituting  the  endo- 
thelial wall  of  a  primitive  blood  channel  (Fig.  25,  C).  Exten- 
sion and  anastomosis  of  neighboring  blood  islands  which  have 
undergone  similar  differentiation  results  in  the  establishment  of 
a  network  of  communicating  vessels.  Meanwhile  the  cells 
enclosed  in  the  primitive  blood  channels  have  become  separated 


STRUCTURE   OF   THIRTY-THREE  HOUR   CHICKS 


67 


from  each  other  and  rounded.  They  soon  come  to  contain 
haemoglobin  and  constitute  the  primitive  blood  corpuscles. 
The  fluid  accumulated  in  the  blood  islands  serves  as  a  vehicle 
in  which  the  corpuscles  are  suspended  and  conveyed  along 
the  vessels. 


yolk 


ectoderm 


central  cells  of 
blood  island 

peripheral  cell 
of  blood  island 


ectoderm 


blood  cells 
entoderm  cell 


somatic 
mesoderm 
coelom 

endothelial  cell 
lumen 

yolk 


Fig.  25. — Drawings  to  show  the  cellular  organization  of  blood  islands  at 
three  stages  in  their  differentiation.  The  location  of  the  areas  drawn  with 
reference  to  the  body  of  the  embryo  and  other  structtires  of  the  blastoderm 
can  be  ascertained  by  reference  to  Fig.  17,  D. 

A,  from  blastoderm  of  18-hour  chick;  B,  from  blastoderm  of  24-hour  chick;. 
C,  from  blastoderm  of  33-hour  chick. 

The  differentiation  of  the  blood  islands  in  the  manner  de- 
scribed begins  first  in  the  peripheral  part  of  the  area  vasculosa 
and  from  there  extends  toward  the  body  of  the  embryo.  By 
33  hours  of  incubation  the  extra-embryonic  vascular  plexus  has 
extended  inward  and  made  connection  with  the  omphalomesen- 
teric veins  which,  originating  within  the  body  of  the  embryo 


68  EARLY   EMBRYOLOGY   OF   THE   CHICK 

have  grown  outward.  Thus  are  established  the  afferent  vitel- 
line channels  (Fig.  21). 

The  efferent  vitelline  channels  have  not  yet  appeared  and 
there  is  no  circulation  of  the  blood  corpuscles  which  are  being 
formed  in  the  area  vasculosa.  Th^  intra-embryonic  blood 
vessels  remain  empty  until  the  extra-embryonic  circuit  is  com- 
pleted. The  embryo  meanwhile  draws  its  nutrition  from  the 
yolk  by  direct  absorption. 

The  Formation  of  the  Heart. — The  structural  relations  of 
the  heart  and  the  way  in  which  it  is  derived  from  the  mesoderm 
can  be  grasped  only  by  the  careful  study  of  sections  through 
the  heart  region  in  several  stages  of  development  (Fig.  26). 
The  fact  that  the  heart,  itself  an  unpaired  structure,  arises 
from  paired  primordia  which  at  first  lie  widely  separated  on 
either  side  of  the  mid-line,  is  likely  to  be  troublesome  unless  its 
significance  is  understood  at  the  outset.  The  paired  condition 
of  the  heart  at  the  time  of  its  origin  is  due  to  the  fa.ct  that  the 
early  embryo  lies  open  ventrally,  spread  out  on  the  yolk  sur- 
face. The  rudiments  of  all  ventral  structures  which  appear  at 
an  early  age  are  thus  at  first  separated,  and  lie  on  either  side 
of  the  mid-line. 

As  the  embryo  develops,  a  series  of  foldings  undercut  it  and 
separate  it  from  the  yolk.  This  folding  off  process  at  the  same 
time  establishes  the  ventral  wall  of  the  gut  and  the  ventral  body 
wall  of  the  embryo  by  bringing  together  in  the  mid-line  the 
structures  formerly  spread  out  to  right  and  left.  The  primordia 
of  the  heart  arise  in  connection  with  layers  which  are  destined 
to  form  ventral  parts  of  the  embryo,  but  at  a  time  when  these 
layers  are  still  spread  out  on  the  yolk.  As  the  embryo  is  com- 
pleted ventrally  the  paired  primordia  of  the  heart  are  brought 
together  in  the  mid-line  and  become  fused  (Fig.  27). 

The  first  indication  of  heart  formation  is  to  be  seen  in  trans- 
verse sections  passing  through  a  2S-hour  chick  immediately 
caudal  to  the  anterior  intestinal  portal.  Where  the  splanchno- 
pleure  of  either  side  bends  toward  the  mid-line  along  the  lateral 
margin  of  the  intestinal  portal  there  is  a  marked  regional  thick- 
ening in  the  splanchnic  mesoderm  of  either  side  (Figs.  26,  A 
and  27,  yl).  This  pair  of  thickenings  indicates  where  there  has 
been  rapid  cell  proliferation  preliminary  to  the  differentiation 
of  the  heart.     Loosely  associated   cells  can  already  be  seen 


STRUCTURE    OF    THIRTY-THREE   HOUR   CHICKS  69 

somewhat  detached  from  the  mesial  face  of  the  mesoderm  layer. 
These  cells  soon  become  organized  to  form  the  endocardial 
primordia. 

In  a  chick  of  about  26  hours,  sections  through  a  corresponding 
region  show  distinct  dfferentiation  of  the  endocardial  and  epi- 
myocardial  primordia  (Fig.  26,  B).  The  endocardial  primordia 
are  a  pair  of  delicate  tubular  structures,  a  single  cell  in  thick- 
ness, lying  between  the  entoderm  and  mesoderm.  They  arise 
from  the  cells  seen  separating  from  the  adjacent  thickened  meso- 
derm in  the  25-hour  chick.  As  their  name  indicates  they  are 
destined  to  give  rise  to  the  endothelial  lining  of  the  heart.  By 
far  the  greater  part  of  each  of  the  original  mesodermic  thicken- 
ings becomes  applied  to  the  lateral  aspects  of  the  endocardial 
tubes  as  the  epi-myocardial  primordium  which  is  destined  to 
give  rise  to  the  external  coat  of  the  heart  (epicardium)  and  to 
the  heavy  muscular  layers  of  the  heart  (myocardium). 

In  chicks  of  27  hours  the  lateral  margins  of  the  anterior  intes- 
tinal portal  have  been  undergoing  concrescence  lengthening 
the  fore-gut  caudally  and  involving  the  heart  region.  In  this 
process  the  former  lateral  margins  of  the  portal  swing  in  to 
meet  each  other  and  fuse  in  the  mid-line,  and  the  endocardial 
tubes  of  the  right  and  left  side  are  brought  toward  each  other 
beneath  the  newly  completed  floor  of  the  fore-gut  (Figs.  26,  C 
and  27,  B).  In  the  28-hour  chick  the  endocardial  primordia 
are  approximated  to  each  other  (Figs.  26,  D  and  27,  C)  and  by  29 
hours  they  fuse  in  their  mid-region  to  form  a  single  tube  (Figs. 
26,  E  and  27,  D). 

At  the  same  time  the  epi-myocardial  areas  of  the  mesoderm 
are  brought  together  first  ventrally  (Fig.  26,  D)  and  then  dor- 
sally  to  the  endocardium  (Fig.  26,  E).  Where  the  splanchnic 
mesoderm  of  the  opposite  sides  of  the  body  comes  together  dor- 
sal and  ventral  to  the  heart  it  forms  double  layered  supporting 
membranes  called  respectively  the  dorsal  mesocardium  and  the 
ventral  mesocardium.  j  The  ventral  mesocardium  is  a  transitory 
structure,  disappearing  almost  as  soon  as  it  is  formed  (Fig.  26, 
E).  The  dorsal  mesocardium,  although  the  greater  part  of  it 
disappears  in  the  next  few  hours  of  incubation,  persists  in  em- 
bryos of  the  stage  under  consideration,  suspending  the  heart 
in  the  pericardial  region  of  the  coelom.  Conditions  reached  in 
the  heart  region  at  33  hours  of  incubation  are  shown  in  section 


70 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


in  Figure  28,  C.     The  heart  here  is  enlarged  and  displaced 
somewhat  to  the  right  of  the  mid-line  but  its  fundamental 


neural  plate  ectoderm 
donal  meaoderm 


■uperficial  ectoderm 
neural  groove 


j —  somatopleure 
splanchnopleure 


splanchnic  mesoderm 


gut  itrnncdiaoely  caudal  to 
anterior  intestinal  portal 


neural  groove 


epi-myocard 


I somatopleure 

\-  splanchnopleure 

myocardium 


endocardium 


gut  immediately  caudal  to 
anterior  intestinal  portal 


dorsal  mesoderm 


fore-gut 


epi-myocardium 

endocardium 


line  of  fusion  of  lateral  margins  of 
anterior  intestinal  portal 


dorsal  mesoderm 


fore-gut 


dorsal   mesocardium 


ventral  mesocardium 


|—  somatopleure 

}-  splanchnopleure 
epi-myocardium 


dorsal  mesoderm 
notochord 


dorsal  mesocardium 


endocardium 


} —  splanchnopleure 


epi-myocardium 


Fig.  26. — Diagrams  of  transverse  sections  through  the  pericardial  region 
of  chicks  at  various  stages  to  show  the  formation  of  the  heart.  For  location  of 
the  sections  consult  Fig.  27. 

A,  at  25  hours;  B,  at  26  hours;  C,  at  27  hours;  D,  at  28  hours;  E,  at  29  hours. 

relations  are  otherwise  the  same  as  in  a  29-hour  embryo  (Fig. 
26,  E). 


STRUCTURE    OF    THIRTY-THREE    HOUR   CHICKS 


71 


The  gross  shape  of  the  heart  and  its  positional  relations 
to  other  structures  are  best  seen  in  entire  embryos.  The  fusion 
of  the  paired  cardiac  primordia  establishes  the  heart  as  a 
nearly  straight  tubular  structure.  It  lies  at  the  level  of  the 
rhombencephalon  in  the  mid-line,  ventral  to  the  fore-gut 
(Fig.  19).     By  ^^  hours  of  incubation  the  mid-region  of  the 

A. 


pericardial 
_  _  _  region  of  coelom  ^ 


epi-myocardium 


margin  of 
•  anterior  intestinal  -  —  -  -  -  y' 
portal 


1*.:\ 


e 


ventral  aortic 
root 


pericardial 
^-•region  of  coelom  -^.^ 


epi-myocardium 
endocardium 


omphalomesenteric 

vein 


Fig.  27, — Ventral-view  diagrams  to  show  the  origin  and  subsequent  fusion 
of  the  paired  primordia  of  the  heart.  The  lines  A,  C,  D,  and  E  indicate  the 
planes  of  the  sections  diagrammed  in  Fig.  26,  A,  C,  D,  E,  respectively. 

A,  chick  of  25  hours;  B,  chick  of  27  hours;  C,  chick  of  28  hours;  D,  chick  of 
29  hours. 

heart  is  considerably  dilated  and  bent  to  the  right  (Fig.  21). 
At  38  hours  the  heart  k  bent  so  far  to  the  right  that  it  extends 
beyond  the  lateral  body  margin  of  the  embryo  (Fig.  22).  This 
bending  process  is  correlated  with  the  rupture  of  the  dorsal 
mesocardium  at  the  mid-r-egion  of  the  heart.     The  breaking 


72  EARLY  EMBRYOLOGY  OF  THE  CHICK 

through  of  the  dorsal  and  ventral  mesocardia  is  of  interest 
aside  from  the  fact  that  it  leaves  the  heart  free  to  undergo 
changes  in  shape.  It  makes  the  right  and  left  ccelomic  cham- 
bers confluent,  the  pericardial  region  thus  being  the  first  part 
of  the  coelom  to  acquire  the  unpaired  condition  characteristic 
of  the  adult. 

Although  there  are  as  yet  no  sharply  bounded  subdivisions  of 
the  heart,  it  is  convenient  to  distinguish  four  regions  which  later 
become  clearly  marked  off  from  each  other  (Fig.  23).  The 
most  caudal  part  of  the  heart  where  the  omphalomesenteric 
veins  join  is  the  sinus  venosus;  the  caudal  part  of  the  region 
of  the  heait  which  is  dilated  and  bent  to  the  right  will  become 
the  atrium;  the  cephalic  part  of  the  heart  bend  is  the  ventricular 
region;  and  the  region  where  the  ventricle  swings  into  the  mid- 
line and  becomes  narrowed  is  known  as  the  bulbo-conus  ar- 
teriosus. Approximately  at  the  stage  of  development  indicated 
in  Figure  23  irregular  twitchings  occur  in  the  heart  walls,  but 
regular  pulsations  are  not  established  until  about  the  44th  hour 
of  incubation. 

The  Formation  of  the  Intra-embryonic  Blood  Vessels. — Co- 
incident with  the  establishment  of  the  heart,  blood  vessels  have 
arisen  within  the  body  of  the  embryo.  Concerning  the  exact 
nature  of  the  process  of  blood  vessel  formation  there  is  some 
disagreement.  The  weight  of  evidence  seems  to  indicate 
that  the  early  vessels  are  formed  from  mesodermal  cells  which 
lie  in  the  path  of  their  development.  They  grow  by  organi- 
zation  of  cells  in  situ  as  a  drain  might  be  built  from  bricks 
already  deposited  along  its  projected  course.  In  later  stages 
it  seems  probable  that  vessels  extend  by  the  formation  of  bud- 
like outgrowths  from  their  walls,  as  well  as  by  organization  of 
cells  in- their  path  of  development.  When  first  formed,  the 
blood  vessel  walls  are  but  a  single  cell  in  thickness.  There 
is  no  structural  differentiation  between  arteries  and  veins 
until  a  considerably  later  period.  Recognition  of  the  vessels 
depends  wholly,  therefore,  on  determining  their  course  and 
relationships. 

The  large  vessels  connecting  with  the  heart  are  the  first  of 
the  intra-embryonic  channels  established.  From  the  bulbo- 
conus  arteriosus  the  paired  ventral  aortic  roots  extend  cephalad 
ventral  to  the  fore-gut  (Fig.  23).    At  the  cephalic  end  of  the 


STRUCTURE   OF   THIRTY-THREE   HOUR   CHICKS 


73 


fore-gut  the  ventral  aortic  roots  turning  dorsad  curve  around 
it,  and  then  extend  caudad,  dorsal  to  the  gut,  as  the  paired 
dorsal  aortae  (Figs.  23,  24  and  Fig.  28,  B).     Few  conspicuous 


ectoderm 
of  blastoderm 


extra-embryonic 
coelom 


mesoderm  1 lateral  plate 

splanchnic  mesoderm  J  of  mesoderm 

Fig.  28. — Diagrams  of  sections  of  33-hour  chick.     The  location  of  each  section 
is  indicated  on  a  small  outline  sketch  of  the  entire  embryo.t 


branches  arise  from  the  aortae  at  this  stage  but  as  development 
"progresses  branches  extend  to  the  various  parts  of  the  embryo 
and  the  aortae  become  the  main  efferent  conducting  vessels  of 


74  EARLY   EMBRYOLOGY   OF   THE   CHICK 

the  embryonic  circulation.  Both  the  ventral  aortic  roots  and 
the  omphalomesenteric  veins  are  direct  continuations  of  the 
paired  endocardial  primordia  of  the  heart.  The  epi-myocardial 
coat  is  formed  about  the  original  endothelial  tubes  only  where 
they  are  fused  in  the  region  destined  to  become  the  heart.  The 
development  of  the  heart  at  this  stage  is  an  epitome  of  its 
phylogenetic  origin.  The  local  investment  of  the  endocardial 
tubes  by  the  epi-myocardium,  as  seen  in  the  formation  of  the 
chick  heart,  is  a  recapitulation  of  the  evolutionary  origin  of 
the  heart  by  the  local  addition  of  a  heavy  muscular  coat  about 
the  walls  of  a  blood  vessel. 

During  early  embryonic  life  the  cardinal  veins  are  the  main 
afferent  vessels  of  the  intra-embryonic  circulation.  The  main 
cardinal  trunks  are  paired  vessels  symmetrically  placed  on 
either  side  of  the  mid-line.  There  are  two  pairs,  the  anterior 
cardinals  which  return  the  blood  to  the  heart  from  the  cephalic 
region  of  the  embryo,  and  the  posterior  cardinals  which  return 
the  blood  from  the  caudal  region.  The  anterior  and  posterior 
cardinal  veins  of  the  same  side  of  the  body  become  confluent 
dorsal  to  the  level  of  the  heart.  The  vessels  formed  by  the 
junction  of  the  anterior  and  posterior  cardinals  are  the  ducts  of 
Cuvier  or  common  cardinal  veins.  The  right  and  left  ducts  of 
Cuvier  turn  ventrad,  one  on  either  side  of  the  fore-gut,  and  enter 
the  sinus-venosus  along  with  the  right  and  left  omphalomesen- 
teric veins,  respectively  (Fig.  24). 

In  chicks  of  33  hours  the  anterior  cardinal  veins  can  usually 
be  made  out  in  sections  (Fig.  28,  B,  C).  By  38  hours  the  an- 
terior cardinals  and  the  ducts  of  Cuvier  are  readily  recognized. 
The  posterior  cardinals  appear  somewhat  later  than  the  an- 
terior cardinals  but  are  ordinarily  discernible  in  the  region  of  the 
duct  of  Cuvier  by  33  to  35  hours  and  well  established  by  38 
hours.  For  the  sake  of  simplicity  and  clearness  the  cardinal 
veins  have  been  represented  in  Figure  24  larger  and  more 
regularly  formed  than  they  are  in  actual  specimens.  Like  all 
the  other  blood  vessels  of  the  embryo  they  arise  as  irregular 
anastomosing  endothelial  tubes,  only  gradually  taking  on  the 
regularity  of  shape  characteristic  of  fully  formed  vessels. 


CHAPTER  X 

THE  CHANGES  BETWEEN  FORTY  AND  FIFTY  HOURS 
OF  INCUBATION 

Flexion  and  torsion;  the  completion  of  the  vitelline 
circulatory  channels;  the  beginning  of  the  circu- 
lation of  blood. 

Flexion  and  Torsion.— Until  36  or  37  hours  of  incubation  the 
longitudinal  axis  of  the  chick  is  straight  except  for  slight  for- 
tuitous variations.  Beginning  at  about  38  hours,  processes  are 
initiated  which  eventually  change  the  entire  configuration  of  the 
embryo  and  its  positional  relations  to  the  yolk.  These  proc- 
esses involve  positional  changes  of  two  distinct  types,  flexion 
and  torsion.  As  applied  to  an  embryo,  flexion  means  the  bend- 
ing of  the  body  about  a  transverse  axis,  as  one  might  bend  the 
head  forward  at  the  neck,  or  the  trunk  forward  at  the  hips. 
Torsion  means  the  twisting  of  the  body,  as  one  might  turn  the 
head  and  shoulders  in  looking  backwards  without  changing  the 
position  of  the  feet. 

In  chick  embryos  the  first  flexion  of  the  originally  straight 
body-axis  takes  place  in  the  head  region.  Because  of  its  loca- 
tion it  is  known  as  the  cranial  flexure.  The  axis  of  bending  in 
the  development  of  the  cranial  flexure  is  a  transverse  axis  pas- 
sing through  the  mid-brain  at  the  level  of  the  anterior  end  of  the 
notochord.  The  direction  of  the  flexion  is  such  that  the 
fore-brain  becomes  bent  ventrally  toward  the  yolk.  The  proc- 
ess is  carried  out  as  if  the  brain  were  being  bent  about  the 
anterior  end  of  the  notochord.  Until  the  cranial  flexure  is  well 
established  it  is  inconspicuous  in  dorsal  views  of  whole-mounts 
but  even  in  its  initial  stages  it  appears  plainly  in  lateral  views 
(Fig.  24). 

To  appreciate  the  correlation  between  the  processes  of  flexion 
and  torsion  it  is  only  necessary  to  bear  in  mind  the  relation  of 
a  chick  of  this  stage  to  the  yolk.  As  long  as  the  chick  lies  with 
its  ventral  surface  closely  applied  to  the  yolk,  the  yolk  consti- 
tutes a  bar  to  flexion.     Before  extensive  flexion  can  be  carried 


76 


EARLY   EMBRYOLOGY    OF   THE    CHICK 


out  the  chick  must  twist  around  on  its  side,  i.e.,  undergo  tor- 
sion, as  a  man  lying  face  down  turns  on  his  side  in  order  to 
flex  his  body. 

Torsion  begins  in  the  cephalic  region  of  the  embryo  and  pro- 
gresses caudad.  The  first  indications  of  torsion  appear  almost 
as  soon  as  the  cranial  flexure  begins  and  the  two  processes  then 
progress  synchronously.  In  the  chick,  torsion  is  normally  car- 
ried out  toward  a  definite  side.     The  cephahc  region  of  the 


mesencephalon 


metencephalon 

myelencephalon 
auditory  pit 

sinus  resion 

somite, 
lateral  mesoderm- 
lateral  body  fold 


unsegmented  dorsal 
mesoderm 


prosencephalon 


optic  vesicle 


margin  of 
head  fold  of  amnion 


bulbo-conus  arteriosus 

ventricular  region 
atrial  region 
omphalomesenteric  vein 


extra-embryonic 
vascular  plexus 


oipphalo  mesenteric 
artery 


neural  tube 


primitive  plate 


Fig.  29. — Dorsal  view  (  X  14)  of  entire  chick  embryo  having  19  pairs  of 
somites  (about  43  hours  incubation).  Due  to  torsion  the  cephalic  region  appears 
in  dextro-dorsal  view. 


embryo  is  twisted  in  such  a  manner  that  the  left  side  comes  to 
lie  next  to  the  yolk  and  the  right  side  away  from  the  yolk. 
The  progress  of  torsion  caudad  is  gradual  and  the  posterior 
part  of  the  embryo  remains  prone  on  the  yolk  for  a  considerable 
time  after  torsion  has  been  completed  in  the  head  region.  Fig- 
ure 22  shows  the  head  of  an  embryo  of  about  38  hours  in  which 
the  cranial  flexure  and  torsion  are  just  becoming  evident.  In 
chicks  of  about  43  hours  (Fig.  29)  the  further  progress  of  both 
flexion  and  torsion  is  well  marked. 

The  processes  of  flexion  and  torsion  thus  initiated  continue 


CHANGES  BETWEEN  40  AND  50  HOURS         77 

until  the  original  orientation  of  the  chick  on  the  yolk  is  com- 
pletely changed.  As  the  body  of  the  embryo  becomes  turned 
on  its  side  the  yolk  no  longer  impedes  the  progress  of  flexion. 
Following  the  accomplishment  of  torsion  in  the  cephaUc  region, 
the  cranial  flexure  becomes  rapidly  greater  until  the  head  is 
practically  doubled  on  itself  (Fig.  34).  As  development  pro- 
ceeds, torsion  progresses  caudad  involving  more  and  more  of 
the  body  of  the  embryo.  Finally  the  entire  embryo  comes  to 
lie  with  its  left  side  on  the  yolk.  Concomitant  with  the  progress 
of  torsion,  flexion  also  appears  farther  caudally,  affecting  in 
turn  the  cervical,  dorsal,  and  caudal  regions.  The  series  of 
flexions  which  accompany  torsion  bend  the  head  and  tail  of 
the  embryo  ventrally  so  that  its  spinal  axis  becomes  C-shaped 
(Fig.  40).  The  flexions  which  bend  the  embryo  on  itself  so 
the  head  and  tail  lie  close  together  are  characteristic  of  all 
amniote  embryos.  The  torsion  which  in  the  chick  accompanies 
flexion  is  correlated  with  the  fact  that  it  develops  on  the  surface 
of  a  large  yolk. 

The  Completion  of  the  Vitelline  Circulatory  Channels. — In 
chicks  of  $$  to  36  hours  the  omphalomesenteric  veins  have  been 
established  as  postero-lateral  extensions  of  the  same  endocardial 
tubes  which  are  involved  in  the  formation  of  the  heart.  As 
the  omphalomesenteric  veins  are  extending  laterad,  the  vessels 
developing  in  the  vitelline  plexus  are  extending  and  converging 
toward  the  embryo.  Eventually  the  vitelline  vessels  attain 
communication  with  the  heart  by  becoming  confluent  with  the 
omphalomesenteric  veins.  This  establishes  the  afferent  chan- 
nels of  the  vitelline  circulation. 

The  vessels  destined  to  carry  blood  from  the  embryo  to  the 
vitelline  plexus  develop  in  embryos  of  about  40  hours  (Fig.  29). 
Like  the  afferent  vitelline  channels,  the  efferent  channels  have 
a  dual  origin.  The  proximal  portions  of  the  efferent  channels 
arise  within  the  embryo  as  branches  of  the  dorsal  aortae,  and 
extend  peripherally.  The  distal  portions  of  the  channels  arise 
in  the  extra-embryonic  vascular  area  and  extend  toward  the 
embryo.  The  efferent  vitelHne  vessels  are  estabhshed  when 
these  two  sets  of  channels  become  confluent.  In  its  early  stages 
the  connection  is  through  a  network  of  small  channels  rather 
than  definite  vessels,  the  aortae  breaking  up  posteriorly  into 
,  small  channels  some  of  which  communicate  laterally  with  the 


78  EARLY  EMBRYOLOGY   OF   THE   CHICK 

extra-embryonic  plexus.  Later  some  of  these  channels  become 
confluent,  others  disappear,  and  gradually  definite  main  vessels, 
the  omphalomesenteric  arteries,  are  estabHshed.  For  some 
time  after  their  formation,  the  omphalomesenteric  arteries  are 
Hkely  to  retain  traces  of  their  origin  from  a  plexus  of  small 
channels  and  arise  from  the  aorta  by  several  roots  (Fig.  35). 

The  Beginning  of  the  Circulation  of  Blood. — At  about  44 
hours  of  incubation,  coincident  with  the  completion  of  the 
vitelline  vessels,  the  heart  begins  regular  contraction,  and  the 
blood  which  has  been  formed  in  the  extra-embryonic  vascular 
area  is  for  the  first  time  pumped  through  the  vessels  of  the 
embryo.  In  tracing  the  course  of  either  the  embryonic  or  the 
vitelline  circulation  the  heart  is  the  logical  starting  point. 
From  the  heart  the  blood  of  the  extra-embryonic  vitelline  circu- 
lation passes  through  the  ventral  aortae,  along  the  dorsal  aortae, 
and  out  through  the  omphalomesenteric  arteries  to  the  plexus 
of  vessels  on  the  yolk. 

In  the  small  vessels  which  ramify  in  the  membranes  envelop- 
ing the  yolk  the  blood  absorbs  food  material.  In  young 
embryos,  before  the  allantoic  circulation  has  appeared,  the 
vitelHne  circulation  is  involved  also  in  the  oxygenation  of  the 
blood.  The  great  surface  exposure  presented  by  the  multitude 
of  small  vessels  on  the  yolk  makes  it  possible  for  the  blood  to 
take  up  oxygen  which  penetrates  the  porous  shell  and  the 
albumen. 

After  acquiring  food  material  and  oxygen  the  blood  is 
collected  by  the  sinus  terminalis  and  the  vitelline  veins.  The 
vitelline  veins  converge  toward  the  embryo  from  all  parts  of 
the  vascular  area  and  empty  into  the  omphalomesenteric  veins 
which  return  the  blood  to  the  heart  (Fig.  48) . 

The  blood  of  the  intra-embryonic  circulation,  leaving  the 
heart  enters  the  ventral  aortae,  thence  passes  into  the  dorsal 
aortae,  and  is  distributed  through  branches  from  the  dorsal 
aortae  to  the  body  of  the  embryo.  It  is  returned  from  the 
cephalic  part  of  the  body  by  the  anterior  cardinals,  and  from 
the  caudal  part  of  the  body  by  the  posterior  cardinals.  The 
anterior  and  posterior  cardinals  discharge  together  through  the 
ducts  of  Cuvier  into  the  sinus  region  of  the  heart  (Fig.  24). 

In  the  heart,  the  blood  of  the  extra-embryonic  circulation 
and  of  the  intra-embryonic  circulation  is  mixed.     The  mixed 


CHANGES  BETWEEN  40  AND  50  HOURS         79 

blood  in  the  heart  is  not  as  rich  in  oxygen  and  food  material  as 
that  which  comes  to  the  heart  from  the  vitelhne  circulation 
nor  as  low  in  food  and  oxygen  content  as  that  returned  to  the 
heart  from  the  intra-embryonic  circulation  where  these  ma- 
terials are  drawn  upon  by  the  growing  tissues  of  the  embryo. 
Nevertheless  it  carries  a  sufficient  proportion  of  food  and  oxygen 
so  that  as  it  is  distributed  to  the  body  of  the  embryo  it  serves  to 
supply  the  growing  tissues. 


CHAPTER  XI 

EXTRA-EMBRYONIC  MEMBRANES 

The  folding  off  of  the  body  of  the  embryo;  the  establish- 
ment OF  THE  YOLK-SAC  AND  THE  DELIMITATION  OF  THE 
EMBRYONIC  GUT;  THE  AMNION  AND  THE  SEROSA;  THE 
ALLANTOIS. 

The  Folding  off  of  the  Body  of  the  Embryo. — In  bird  embryos 
the  somatopleure  and  splanchnopleure  extend  over  the  yolk 
peripherally,  beyond  the  region  where  the  body  of  the  embryo 
is  being  formed.  Distal  to  the  body  of  the  embryo  the  layers 
are  termed  extra-embryonic.  At  first  the  body  of  the  chick  has 
no  definite  boundaries  and  consequently  embryonic  and  extra- 
embryonic layers  are  directly  continuous  without  there  being 
any  definite  boundary  at  which  we  may  say  one  ends  and  the 
other  begins.  As  the  body  of  the  embryo  takes  form,  a  series 
of  folds  develop  about  it,  undercut  it,  and  finally  nearly  separate 
it  from  the  yolk.  The  folds  which  thus  definitely  estabHsh  the 
boundaries  between  intra-embryonic  and  extra-embryonic 
regions  are  known  as  the  limiting  body  folds  or  simply  the  body 
folds. 

The  first  of  the  body  folds  to  appear  is  the  fold  which  marks 
the  boundary  of  the  head.  By  the  end  of  the  first  day  of  incu- 
bation the  head  has  grown  anteriorly  and  the  fold  originally 
bounding  it  appears  to  have  undercut  and  separated  it  anteriorly 
from  the  blastoderm  (Figs.  15  and  17,  E).  The  cephalic  limit- 
ing fold  at  this  stage  is  crescentic,  concave  caudally.  As  this 
fold  continues  to  progress  caudad,  its  posterior  extremities 
become  continuous  with  folds  which  develop  along  either  side  of 
the  embryo.  Because  of  the  fact  that  these  folds  bound 
the  body  of  the  embryo  laterally,  they  are  known  as  the  lateral 
bod}'  folds  (lateral  hmiting  sulci).  The  lateral  body  folds,  at 
first  shallow  (Fig.  28,  D)  become  deeper,  undercutting  the  body 
of  the  embryo  from  either  side  and  further  separating  it  from 
the  yolk  (Fig.  36,  £  and  Fig.  30). 

80 


EXTRA-EMBRYONIC    MEMBRANES  8 1 

During  the  third  day  a  fold  appears  bounding  the  posterior 
region  of  the  embryo  (Fig.  31,  C).  This  caudal  fold  undercuts 
the  tail  of  the  embryo  forming  a  sub  caudal  pocket  just  as  the 
sub-cephaHc  fold  undercuts  the  head.  The  combined  effect  of 
the  development  of  the  sub-cephahc,  lateral  body,  and  the  sub- 
caudal  folds  is  to  constrict  off  the  embryo  more  and  more  from 
the  yolk  (Figs.  30  and  32).  These  folds  which  establish  the 
contour  of  the  embryo  indicate  at  the  same  time  the  boundary 
between  the  tissues  which  are  built  into  the  body  of  the  embryo, 
and  the  so-called  extra-embryonic  tissues  which  serve  temporary 
purposes  during  development  but  are  not  incorporated  in  the 
structure  of  the  adult  body. 

The  Establishment  of  the  Yolk-sac  and  the  Delimitation  of 
the  Embryonic  Gut. — The  extra-embryonic  membranes  of  the . 
chick  are  four  in  number,  the  yolk-sac,  the  amnion,  the  serosa 
and  the  allantois.  The  yolk-sac  is  the  first  of  these  to  make  its 
appearance.  The  splanchnopleure  of  the  chick  instead  of 
forming  a  closed  gut,  as  happens  in  forms  with  little  yolk, 
grows  over  the  yolk  surface.  The  primitive  gut  has  a  cellular 
wall  dorsally  only,  while  the  yolk  acts  as  a  temporary  floor 
(Fig.  31,  ^).  The  extra-embryonic  extension  of  the  splanchno- 
pleure eventually  forms  a  sac-like  investment  for  the  yolk 
(Figs.  30  and  32). 

Concomitant  with  the  spreading  of  the  extra-embryonic 
splanchnopleure  about  the  yolk,  the  intra-embryonic  splanchno- 
pleure is  undergoing  a  series  of  changes  which  result  in  the 
establishment  of  a  completely  walled  gut  in  the  body  of  the 
embryo.  The  interrelations  of  the  various  steps  in  the  forma- 
tion of  the  gut  and  of  the  yolk-sac  make  it  necessary  to  repeat 
some  points  and  anticipate  other  points  concerning  the  forma- 
tion of  the  gut,  in  order  that  their  relation  to  yolk-sac  formation 
may  not  be  overlooked. 

It  will  be  recalled  that  the  first  part  of  the  primitive  gut  to 
acquire  a  cellular  floor  is  its  cephalic  region.  The  same  folding 
process  by  which  the  head  is  separated  from  the  blastoderm 
involves  the  entoderm  of  the  gut.  The  part  of  the  primitive 
gut  which  acquires  a  floor  as  the  sub-cephalic  fold  progresses 
caudad  is  termed  the  fore-gut  (Fig.  31,  B).  During  the  third 
day  of  incubation  the  caudal  fold  undercuts  the  posterior  end  of 
the   embryo.     The   splanchnopleure   of   the   gut   is   involved 


82 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


embryo 


lateral  amniotic  fold 
lateral  body  fold 

ex -embryonic 
coelom 


ectoderm  ^ 
mesoderm  J 


mes") 


pleure 

splanch- 
hopleure 


yolk 


amniotic  cavity 


lateral 
amniotic  fold 

amnion 
/  somatopleure) 
serosa 
Tsomatopleure) 


embryo 


allantois  (  splanchnopleure  ) 
yolk  stalk 

yolk-sac 
/splanch- 
nopleure \ 


albumen 


vitelline  membrane 


Fig.  30. 


EXTRA-EMBRYONIC   MEMBRANES 


83 


allantoic  cavity 


allantois 


amnion 
amniotic 


extra-embryonic 
coelom 


somatopleure 


yolk-sac 
/  splanchno- 
pleure ) 

albumen 


allantoic  cavity 

allantois 
serosa 


shell 


sero-ammotic 
cavity 


yolk-sac 


albumen 


vitelline 
membrane 


belly    stalk 


Fig.  30. — Schematic  diagrams  to  show  the  extra-embryonic  membranes 
of  the  chick.  {After  Duval.)  The  diagrams  represent  longitudinal  sections 
through  the  entire  egg.  The  body  of  the  embryo,  being  oriented  approximately 
at  right  angles  to  the  long-axis  of  the  egg,  is  cut  transversely. 

A,  embryo  of  about  two  days  incubation;  B,  embryo  of  about  three  days 
incubation;  C,  embryo  of  about  five  days  incubation;  D,  embryo  of  about  fourteen 
days  incubation. 


•84  EARLY   EMBRYOLOGY    OF    THE   CHICK 

in  the  progress  of  the  sub-caudal  fold  so  that  a  hind-gut  is 
established  in  a  manner  analogous  to  the  formation  of  the  fore- 
gut  (Fig.  31,  C).  The  part  of  the  gut  which  still  remains  open 
to  the  yolk  is  known  as  the  mid-gut.  As  the  embryo  is  con- 
stricted off  from  the  yolk  by  the  progress  of  the  sub-cephalic 
and  sub-caudal  folds,  the  fore-gut  and  hind-gut  are  increased  in 
extent  at  the  expense  of  the  mid-gut.  The  mid-gut  is  finally 
diminished  until  it  opens  ventrally  by  a  small  aperture  which 
flares  out,  like  an  inverted  funnel,  into  the  yolk-sac  (Fig.  31,  Z)). 
This  opening  is  the  yolk  duct  and  its  wall  constitutes  the  yolk 
stalk. 

The  walls  of  the  yolk-sac  are  still  continuous  with  the  walls 
of  the  gut  along  the  constricted  yolk-stalk  thus  formed,  but  the 
boundary  between  the  intra-embryonic  splanchnopleure  of  the 
gut  and  the  extra-embryonic  splanchnopleure  of  the  yolk-sac 
can  now  be  established  definitely  at  the  yolk-stalk. 

As  the  neck  of  the  yolk-sac  is  constricted  the  omphalomesen- 
teric arteries  and  omphalomesenteric  veins,  caught  in  the  same 
series  of  foldings,  are  brought  together  and  traverse  the  yolk- 
stalk  side  by  side.  The  vascular  network  in  the  splanchno- 
pleure of  the  yolk-sac  which  in  young  chicks  was  seen  spreading 
over  the  yolk  eventually  nearly  encompasses  it.  The  embryo's 
store  of  food  material  thus  comes  to  be  suspended  from  the  gut 
of  the  mid-body  region  in  a  sac  provided  with  a  circulatory  arc 
of  its  own,  the  vitelline  arc.  Apparently  no  yolk  passes  directly 
through  the  yolk-duct  into  the  intestine.  Absorption  of  the 
yolk  is  effected  by  the  epithelium  of  the  yolk-sac  and  the  food 
material  is  transferred  to  the  embryo  by  the  vitelline  circula- 
tion. In  older  embryos  (Fig.  30,  C  and  D)  the  epithelium  of 
the  yolk-sac  undergoes  a  series  of  foldings  which  greatly  increase 
its  surface  area  and  thereby  the  amount  of  absorption  it  can 
accomplish. 

During  development  the  albumen  loses  water,  becomes 
more  viscid ,  and  rapidly  decreases  in  bulk.  The  growth  of  the 
allantois,  an  extra-embryonic  structure  which  we  have  yet  to 
consider,  forces  the  albumen  toward  the  distal  end  of  the  yolk- 
sac  (Fig.  30,  D).  The  manner  in  which  the  albumen  is  encom- 
passed between  the  yolk-sac  and  folds  of  the  allantois  and 
serosa  belong  to  later  stages  of  development  than  those  with 
which  we  are  concerned.     Suffice  it  to  say  that  the  albumen 


EXTEA-EMBRYONIC   MEMBRANES 


85 


ectoderm  of  neural  plate 
ectoderm  of  blastoderm 


primitive  pit 

primitive  streak 


yolk 


lii-^v^r^ 


w&mmm^^^'^^mi^ii'^f^:^  ?  '^ 


fore-gut 


neural   tube 
ectoderm  of  head 

subcephalic  pocket 

splanchnopleure; 
of  yolk-sac 


open  neural  groove 
primitive  pit 


B  pericardial  region '  anterior  intestinal 

of  coelom 


portal 


fore-gut 


subcephalic  pocket 


extra-embryonic 
coelom 


•»  ■d*'do*<'o''. 


antenor  posterior 

intestinal  portal         intestinal  portal 


hind-gur 


subcaudal  pocket 

)-  amnion 
—  extra-embryonic 
■3^:5;;^  coelom 


splanchnopleure 
of  yolk-sac 


post-anal  gut 
proctodaeum 


mid-gut 


splanchnopleure 
of  yolk-sac 


allantoic  bud 
yolk-  stalk 


Fig.  31. — Schematic  longitudinal-section  diagrams  of  the  chick  showing: 
four  stages  in  the  formation  of  the  gut  tract.  The  embryos  are  represented  as 
unaffected  by  torsion. 

A,  chick  toward  the  end  of  the  first  day  of  incubation;  no  regional  differentia- 
tion of  primitive  gut  is  as  yet  apparent.  B,  toward  the  end  of  the  second  day^ 
fore-gut  established.  C,  chick  of  about  three  days;  fore-gut,  mid-gut  and  hind- 
gut  established.  D,  chick  of  about  four  days;  fore-gut  and  hind-gut  increased 
in  length  at  expense  of  mid-gut;  yolk-stalk  formed. 


86  EARLY   EMBRYOLOGY   OF   THE   CHICK 

like  the  yolk,  is  surrounded  by  extra-embryonic  membranes  by 
which  it  is  absorbed  and  transferred  over  the  extra-embryonic 
circulation  to  the  embryo. 

Toward  the  end  of  the  period  of  incubation,  usually  on  the 
19th  day,  the  remains  of  the  yolk-sac  are  enclosed  within  the 
body  walls  of  the  embryo.  After  its  inclusion  in  the  embryo 
both  the  wall  and  the  remaining  contents  of  the  yolk-sac 
rapidly  disappear,  their  absorption  being  practically  completed 
in  the  first  six  days  after  hatching. 

The  Amnion  and  the  Serosa. — The  amnion  and  the  serosa 
are  so  closely  associated  in  their  origin  that  they  must  be  con- 
sidered together.  Both  are  derived  from  the  extra-embryonic 
somatopleure.  The  amnion  encloses  the  embryo  as  a  saccular 
investment  and  the  cavity  thus  formed  between  the  amnion 
and  the  embryo  becomes  filled  with  a  watery  fluid.  Suspended 
in  this  amniotic  fluid,  the  embryo  is  free  to  change  its  shape 
and  position,  and  external  pressure  upon  it  is  equalized.  Mus- 
cle fibers  develop  in  the  amnion,  which  by  their  contraction 
gently  agitate  the  amniotic  fluid.  The  movement  thus  im- 
parted to  the  embryo  apparently  aids  in  keeping  it  free  and 
preventing  adhesions  and  resultant  malformations. 

The  first  indication  of  amnion  formation  appears  in  chicks 
of  about  30  hours  incubation.  The  head  of  the  embryo  sinks 
into  the  yolk  somewhat,  and  at  the  same  time  the  extra-embry- 
onic somatopleure  anterior  to  the  head  is  thrown  into  a  fold, 
the  head  fold  of  the  amnion  (Fig.  32,-4).  In  dorsal  aspect  the 
margin  of  this  fold  is  crescentic  in  shape  with  its  concavity 
directed  toward  the  head  of  the  embryo.  The  head  fold  of  the 
amnion  must  not  be  confused  with  the  sub-cephalic  fold  which 
arises  earlier  in  development  and  undercuts  the  head. 

As  the  embryo  increases  in  length  its  head  grows  anteriorly 
into  the  amniotic  fold.  Growth  in  the  somatopleure  itself 
tends  to  extend  the  amniotic  fold  caudad  over  the  head  of  the 
embryo  (Fig.  32,  B).  By  continuation  of  these  two  growth 
processes  the  head  soon  comes  to  lie  in  a  double  walled  pocket 
of  extra-embryonic  somatopleure  which  covers  the  head  like  a 
cap  (Fig.  29).  The  free  edge  of  the  amniotic  pocket  retains 
its  original  crescentic  shape  as,  in  its  progress  caudad,  it  covers 
more  and  more  of  the  embryo. 


EXTRA-EMBRYONIC   MEMBRANES  87 

The  caudally-directed  limbs  of  the  head  fold  of  the  amnion 
are  continued  posteriorly  along  either  side  of  the  embryo  as 
the  lateral  amniotic  folds.  The  lateral  folds  of  the  amnion 
grow  dorso-mesiad,  eventually  meeting  in  the  mid-line  dorsal 
to  the  embryo  (Fig.  30,  A-C). 

During  the  third  day,  the  tail-fold  of  the  amnion  develops 
about  the  caudal  region  of  the  embryo.  Its  manner  of  de- 
velopment is  similar  to  that  of  the  head  fold  of  the  amnion 
but  its  direction  of  growth  is  reversed,  its  concavity  being 
directed  anteriorly  and  its  progression  being  cephalad  (Fig. 
32,  B,  C). 

Continued  growth  of  the  head,  lateral,  and  tail  folds  of  the 
amnion  results  in  their  meeting  above  the  embryo.  At  the 
point  where  the  folds  meet,  they  become  fused  in  a  scar-like 
thickening  termed  the  amniotic  raphe  (sero-amniotic  raphe). 
(Fig.  32,  C).  The  way  in  which  the  somatopleure  has  been 
folded  about  the  embryo  leaves  the  amniotic  cavity  completely 
lined  by  ectoderm  which  is  continuous  with  the  superficial 
ectoderm  of  the  embryo  at  the  region  where  the  yolk-stalk 
enters  the  body  (Fig.  30,  D). 

All  the  amniotic  folds  involve  doubling  the  somatopleure  on 
itself.  Only  the  inner  layer  of  the  somatopleuric  fold  is  in- 
volved in  the  formation  of  the  amniotic  cavity.  The  outer 
layer  of  somatopleure  becomes  the  serosa  (Fig.  30,  B).  The 
cavity  between  serosa  and  amnion  (sero-amniotic  cavity)  is  part 
of  the  extra-embryonic  coelom.  The  continuity  of  the  extra- 
embryonic coelom  with  the  intra-embryonic  ccelom  is  most 
apparent  in  early  stages  (Fig.  30,  A  and  B).  They  remain, 
however,  in  open  communication  in  the  yolk-stalk  region  until 
relatively  late  in  development. 

The  rapid  peripheral  growth  of  the  somatopleure  carries  the 
serosa  about  the  yolk-sac,  which  it  eventually  envelops.  The 
albumen-sac  also  is  surrounded  by  folds  of  serosa,  and  the 
allantois  after  its  establishment  develops  within  the  serosa, 
between  it  and  the  amnion.  Thus  the  serosa  eventually 
encompasses  the  embryo  itself  and  all  the  other  extra-embryonic 
membranes.  The  relationships  of  the  serosa  and  allantois 
and  the  functional  significance  of  the  serosa  will  be  taken  up 
after  the  allantois  has  been  considered. 


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EARLY   EMBRYOLOGY   OF   THE    CHICK 


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go  EARLY  EMBRYOLOGY  OF  THE  CHICK 

The  Allantois. — The  allantois  differs  from  the  amnion  and 
serosa  in  that  it  arises  primarily  within  the  body  of  the  embryo. 
Its  proximal  portion  is  intra-embryonic  throughout  develop- 
ment. Its  distal  portion,  however,  is  carried  outside  the  con- 
fines of  the  intra-embryonic  coelom  and  becomes  associated  with 
the  other  extra-embryonic  membranes.  Like  the  other  extra- 
embryonic membranes  the  distal  portion  of  the  allantois 
functions  only  during  the  incubation  period  and  is  not  incorpor- 
ated into  the  structure  of  the  adult  body. 

The  allantois  first  appears  late  in  the  third  day  of  incubation. 
It  rises  as  a  diverticulum  from  the  ventral  wall  of  the  hind-gut 
and  its  walls  are,  therefore,  splanchnopleure.  Its  relationships 
to  structures  within  the  embryo  will  be  better  understood  when 
chicks  of  three  and  four  days  incubation  have  been  studied,  but 
its  general  location  can  be  appreciated  from  the  schematic 
diagrams  of  Figures  32  and  33. 

During  the  fourth  day  of  development  the  allantois  pushes 
out  of  the  body  of  the  embryo  into  the  extra-embryonic  coelom. 
Its  proximal  portion  Hes  parallel  to  the  yolk-stalk  and  just 
caudal  to  it.  When  the  distal  portion  of  the  allantois  has 
grown  clear  of  the  embryo  it  becomes  enlarged  (Fig.  32,  C). 
Its  narrow  proximal  portion  is  known  as  the  allantoic  stalk, 
the  enlarged  distal  portion  as  the  allantoic  vesicle.  Fluid 
accumulating  in  the  allantois  distends  it  so  the  appearance  of 
its  terminal  portion  in  entire  embryos  is  somewhat  balloon-like 
(Fig.  40). 

The  allantoic  vesicle  enlarges  very  rapidly  from  the  fourth 
to  the  tenth  day  of  incubation.  Extending  into  the  sero- 
amniotic  cavity  it  becomes  flattened  and  finally  encompasses 
the  embryo  and  the  yolk-sac  (Fig.  30,  C,  D).  In  this  process 
the  mesodermic  layer  of  the  allantois  becomes  fused  with  the 
adjacent  mesodermic  layer  of  the  serosa.  There  is  thus  formed 
a  double  layer  of  mesoderm,  the  serosal  component  of  which  is 
somatic  mesoderm  and  the  allantoic  component  of  which  is 
splanchnic  mesoderm.  In  this  double  layer  of  mesoderm  an 
extremely  rich  vascular  network  develops  which  is  connected 
with  the  embryonic  circulation  by  the  allantoic  arteries  and 
veins.  It  is  through  this  circulation  that  the  allantois  carries 
on  its  primary  function  of  oxygenating  the  blood  of  the  embryo 
and  relieving  it  of  carbon  dioxide.     This  is  made  possible  by  the 


EXTRA-EMBRYONIC   ME  MBR ANE  S 


91 


position  occupied  by  the  allantois,  close  beneath  the  porous 
shell  (Fig.  30).  In  addition  to  its  primary  respiratory  function 
the  allantois  serves  as  a  reservoir  for  the  secretions  coming  from 


neural   tube 
notochord 


amniotic  cavity 


sero-amniotic  cavity 
hind- gut 


proctodaeum 


' f« 


neural  tube  - 
notochord - 


mesenchyme :^'~*-^"'~ -"*^«  ^V- 

mid-gut 
entoderm 
splanchnic 
mesoderm  • 


yolk  stalk If"'-       If 

#if 

If             11 

If 

[1 

j^M'^%< 

1 

wt- 

V 

\ic 

yolk-sac-p^p^^  ^"  J.^'^'^v;^^:^*,^ 

^ 

^ 

Mf     , a'^  «* jr\  0  •'.  -f  ' d^'6'- '*■'''■  ,"   " '  0 

0" 

u  j^^;jjj^:^£,^^m 

^  . 

,0     -0: 

amniotic  cavity 
cloaca 


.  cloaca  1 

membrane 


post-anal 
gut 


sero-amniotK 
cavity 


proctodaeum 


Pig.  33. — Schematic  longitudinal-section  diagrams  of  the  caudal  half  of  the 
embryo  to  show  the  formation  of  the  allantois. 
A,  chick  of  about  three  days  incubation;  B,  chick  of  about  four    lays  in- 
cubation. 


the  developing  excretory  organs  and  also  takes  part  in  the  ab- 
sorption of  the  albumen. 

The  fusion  of  the  allantoic  mesoderm   and  blood  vessels 


92  EARLY  EMBRYOLOGY   OF   THE   CHICK 

with  the  serosa  is  of  particular  interest  because  of  its  homology 
with  the  establishment  of  the  chorion  in  the  higher  mammals.^ 
The  chorion  of  mammalian  embryos  arises  by  the  fusion  of 
allantoic  vessels  and  mesoderm  with  the  inner  wall  of  the 
serosa,  and  constitutes  the  embryos's  organ  of  attachment  to 
the  uterine  wall.  In  mammalian  embryos  the  allantoic,  or 
umbiUcal  circulation  as  it  is  usually  called  in  mammals,  serves 
more  than  a  respiratory  function.  In  the  absence  of  any 
appreciable  amount  of  yolk,  the  mammalian  embryo  derives  its 
nutrition  through  the  allantoic  circulation  from  the  uterine 
blood  of  the  mother.  Thus  the  mammalian  allantoic  circula- 
tion carries  out  the  functions  which  in  the  chick  are  divided 
between  the  vitelhne  and  the  allantoic  circulations. 

*  By  reason  of  this  homology  the  serosa  of  the  chick  is  sometimes  called  chorion. 
It  seems  less  likely  to  lead  to  confusion  if  the  use  of  the  term  chorion  is  re- 
stricted to  mammalian  forms,  especially  as  the  serosa  alone  is  the  homologue 
of  only  part  of  the  mammalian  chorion.  In  some  books  the  term  outer  or  false 
amnion  will  be  found  used  to  designate  the  structure  called  serosa  in  this  book. 
The  term  false  amnion  is  not,  however,  in  general  use  in  this  country. 


CHAPTER  XII 

THE  STRUCTURE  OF  CHICKS  FROM  FIFTY  TO  FIFTY- 
FIVE  HOURS  OF  INCUBATION 

I.  External  Features. 
II.  The  Nervous  System. 

Growth  of  the  telencephahc  region;  the  epiphysis;  the 
infundibulum  and  Rathke's  pocket;  the  optic  vesicles; 
the  lens;  the  posterior  part  of  the  brain  and  the  cord 
region  of  the  neural  tube;  the  neural  crest. 

III.  The  Digestive  Tract. 

The  fore-gut;  the  stomodaeum;  the  pre-oral  gut;  the 
mid-gut;  the  hind-gut. 

IV.  The  Visceral  Clefts  and  Visceral  Arches. 
V.  The  Circulatory  System. 

The  heart;  the  aortic  arches;  the  fusion  of  the  dorsal 
aortae;  the  cardinal  and  omphalomesenteric  vessels. 
VI.  The  Differentiation  of  the  Somites. 
VII.  The  Urinary  System. 

I.  External  Features 

In  chicks  which  have  been  incubated  from  50  to  55  hours 
(Fig.  34)  the  entire  head  region  has  been  freed  from  the  yolk 
by  the  progress  caudad  of  the  sub-cephalic  fold.  Torsion  has 
involved  the  whole  anterior  half  of  the  embryo  and  is  completed 
in  the  cephalic  region,  so  that  the  head  now  lies  left  side  down 
on  the  yolk.  The  posterior  half  of  the  embryo  is  still  in  its 
original  position,  ventral  surface  prone  on  the  yolk.  At  the 
extreme  posterior  end,  the  beginning  of  the  caudal  fold  marks 
off.  the  tail  region  of  the  embryo  from  the  extra-embryonic  mem- 
branes. The  head  fold  of  the  amnion  has  progressed  caudad, 
together  with  the  lateral  amniotic  folds  impocketing  the  em- 
bryo nearly  to  the  level  of  the  omphalomesenteric  arteries. 

The  cranial  flexure,  which  was  seen  beginning  in  chicks  of 
about  38  hours,  has  increased  rapidly  until  at  this  stage  the 
brain  is  bent  nearly  double  on;  itself.     The  axis  of  the  bending 

93 


94 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


being  in  the  mid-brain  region,  the  mesencephalon  comes 
to  be  the  most  anteriorly  located  part  of  the  head  and  the 
prosencephalon  and  myelencephalon  lie  opposite  each  other, 
ventral  surface  to  ventral  surface  (Fig.  34).  The  original  an- 
terior end  of  the  prosencephalon  is  thus  brought  in  close 
proximity  to  the  heart,  and  the  optic  vesicles  and  the  auditory 
vesicles  are  brought  opposite  each  other  at  nearly  the  same 
antero-posterior  level. 


mesencephalon 


metencephaMc  region 
dorsal  aortic  root 
myelencephahc  region 

hyomandibular  cleft 
auditory  vesicle 
aortic  archill 


anL  int.  nnyfal 


optic  cup 
/lens 


epiphysis 

choroid  fissure 

prosencephalon. 


bulbo-conus 
arteriosus 
atrium 


lateral  mesoderm 
marginof  amnion 
lateral  body  fold 

neural  tube 
,29th  somite 


omphalomesenterif 
artery 


caudal  fold 


Pig.  34. — Dextro-dorsal  view  (  X  14)  of  entire  embryo  of  29  somites  (about 
55  hours  incubation). 


At  this  stage  flexion  has  involved  the  body  farther  caudally 
as  well  as  in  the  brain  region.  It  is  especially  marked  at 
about  the  level  of  the  heart  in  the  region  of  transition  from 
myelencephalon  to  spinal  cord.  Since  this  is  the  future  neck 
region  of  the  embryo  the  flexure  at  this  level  is  known  as  the 
cervical  flexure  (Fig.  34). 


STRUCTURE    OF   FIFTY-HOUR   CHICKS  95 

II.  The  Nervous  System 

Growth  of  the  Telencephalic  Region. — The  completion  of 
torsion  in  the  head  region  causes  rapid  changes  in  the  configura- 
tion of  the  brain  as  seen  in  entire  embryos  from  40  to  50  hours 
of  incubation.  The  same  fundamental  regions  can,  however, 
be  identified  throughout  this  range  of  development.  The  an- 
terior part  of  the  brain  has  undergone  rapid  enlargement.  A 
slight  constriction  in  the  dorsal  wall  (Fig.  35)  indicates  the 
impending  division  of  the  prosencephalon  into  telencephalon 
and  diencephalon.  Except  for  its  considerable  increase  in  size 
no  important  changes  have  taken  place  in  the  telencephalic 
region. 

The  Epiphysis. — In  the  mid-dorsal  waU  of  the  diencephalic 
region  a  small  evagination  has  appeared.  This  evagination  is 
the  epiphysis  (Fig.  34  and  35).  It  is  destined  to  become  dif- 
ferentiated into  the  pineal  gland  of  the  adult. 

The  Infimdibulum  and  Rathke's  Pocket. — In  the  floor  of  the 
diencephalon  the  infundibular  depression  has  become  deepened 
and  Hes  close  to  a  newly  formed  ectodermal  invagination  known 
as  Rathke's  pocket  (Fig.  35).  The  epithelium  of  Rathke's 
pocket  is  destined  to  be  separated  from  the  superficial  ectoderm 
and  to  become  permanently  associated  with  the  infundibular 
portion  of  the  diencephalon  to  form  the  hypophysis  or  pituitary 
body. 

The  Optic  Vesicles. — The  optic  vesicles  have  undergone 
changes  which  completely  alter  their  appearance.  In  33-hour 
chicks  they  are  spheroidal  vesicles  connected  by  broad  stalks 
with  the  lateral  walls  of  the  diencephalon  (Fig.  21).  At  this 
stage  the  lumen  of  each  optic  vesicle  (opticoele)  is  widely  con- 
tinuous with  the  lumen  of  the  prosencephalon  (prosoccele) 
(Fig.  28,  A).  The  constriction  of  the  optic  stalk  which  begins 
to  be  apparent  in  38-hour  embryos  (Fig.  22)  is  much  more 
marked  in  55-hour  chicks. 

The  most  striking  and  important  advance  in  their  develop- 
ment is  the  invagination  of  the  distal  ends  of  the  single-walled 
optic  vesicles  to  form  double  walled  optic  cups  (Fig.  ^6,  B). 
The  concavities  of  the  cups  are  directed  laterally.  Mesially 
the  cups  are  continuous  with  the  ventro-lateral  walls  of  the 
diencephalic  region  of  the  original  prosencephalon  over  the 


96 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


narrowed  optic  stalks.  The  invaginated  layer  of  the  optic  cup 
is  termed  the  sensory  layer  because  it  is  destined  to  give  rise 
to  the  sensory  layer  of  the  retina.     The  layer  against  which 


prosencephalon 
choroid  fissure 
Rathke's  pocket 


ventral  aortic  root- 


anterior  intestinal 
portal 


mesencephalon 

cut  ectoderm 

metencephalon 

anterior  cardinal  vein 
myelencephalon 

neuromere  of 

myelencephalon 
auditory  vesicle 

aortic  arches  I. II, III. 
pharynx 

duct  of  Cuvier 
posterior  cardinal  vein 
dorsal  aorta 

omphalomesenteric  vein 


cut  splanchnopleure 
cut  somatopleure 


roots  of  oinphal( 
mesenteric  artery 


lateral  mesoderm 


om  phjjomesenter  ic 
artery 


posterior  intestinal 
portal 


Fig.  35. — Diagram  of  dissection  of  chick  of  about  50  hours.  (Modified  from 
Prentiss.)  The  splanchnopleure  of  the  yolk-sac  cephalic  to  the  anterior  in- 
testinal portal,  the  ectoderm  of  the  left  side  of  the  head,  and  the  mesoderm  in 
the  pericardial  region  have  been  dissected  away.  A  window  has  been  cut  in 
the  splanchnopleure  of  the  dorsal  wall  of  the  mid-gut  to  show  the  origin  of  the 
omphalomesenteric  arteries. 

the  sensory  layer  comes  to  lie  after  its  invagination  is  termed 
the  pigment  layer  because  it  gives  rise  to  the  pigmented  layer 
of  the  retina.     The  double-walled  cups  formed  by  invagination, 


STRUCTURE    OF   FIFTY-HOUR   CHICKS 


97 


are  also  termed  secondary  optic  vesicles  in  distinction  to  prim- 
ary optic  vesicles,  as  they  are  called  before  the  invagination. 
The  formerly  capacious  lumen  of  the  primary  optic  vesicle  is 


visceral  furrow 


sero- amniotic 
cavity 


fore-gut 

intra-embryonic  coelom 

dorsal  mesocardium 
sero-amniotic  raphe 


extra-embryonic 
coelom 


epi-myocardium  of 
ventricle 

somatopleure 

splanchnopleure 

vitelline  vessels 
extra-embryonic   coelom 


atnum 


neural  crest 

dorsal  aorta 

post,  cardinal  v. 


•embryonic    coelom 
intra-embryonic  coelom 
omphalomesenteric  vein 


lateral  amniotic  fold 
amnion 
serosa 


mesonephric  duct 
mesonephric  tubule 
mid-gut 


lateral 
body  fold 


telline  vessels 

mesonephric  duct '' 

mesonephric  tubule 


post,  cardinal 
dorsal  aorta 


Fig.  36. — Diagrams  of  transverse  sections  of  5S-hour  (30-somite)  chick.     The 
location  of  the  sections  is  indicated  on  an  outline  sketch  of  the  entire  embryo. 


practically  obliterated  in  the  formation  of  the  optic  cup.     What 
remains  of  the  primary  opticoele  is  now  but  a  narrow  space  be- 


98  EARLY   EMBRYOLOGY   OF   THE   CHICK 

tween  the  sensory  and  the  pigment  layers  of  the  retina  (Fig. 
36,  B).  ■  Later  when  these  two  layers  fuse  this  space  is  entirely 
obliterated. 

While  the  secondary  optic  vesicles  are  usually  spoken  of  as 
the  optic  cups,  they  are  not  complete  cups.  The  invagination 
which  gives  rise  to  the  secondary  optic  vesicles,  instead  of  be- 
ginning at  the  most  lateral  point  in  the  primary  optic  vesicles, 
begins  at  a  point  somewhat  toward  their  ventral  surface  and  is 
directed  mesiodorsad.  As  a  result  the  optic  cups  are  formed 
without  any  lip  on  their  ventral  aspect.  They  may  be  likened 
to  cups  with  a  segment  broken  out  of  one  side.  This  gap  in 
the  optic  cup  is  the  choroid  fissure  (Fig.  35).  In  Figure  36,  By 
a  section  is  shown  which  passes  through  the  head  of  the  embryo 
on  a  slight  slant  so  that  the  right  optic  cup,  being  cut  to  one 
side  of  the  choroid  fissure  appears  complete  while  the  left  optic 
cup  being  cut  in  the  region  of  the  fissure  shows  no  ventral  lip. 

The  infolding  process  by  which  the  optic  cups  are  formed 
from  the  primary  optic  vesicles  is  continued  to  the  region  of 
the  optic  stalks.  As  a  result  the  optic  stalks  are  infolded  so 
that  their  ventral  surfaces  become  grooved.  Later  in  develop- 
ment the  optic  nerves  and  blood  vessels  come  to  lie  in  the 
grooves  thus  formed  in  the  optic  stalks. 

The  Lens. — The  lens  of  the  eye  arises  independently  of  the 
optic  vesicles,  from  the  superficial  ectoderm  of  the  head.  The 
first  indications  of  lens  formation  appear  in  chicks  of  about 
40  hours  as  local  thickenings  of  the  ectoderm  immediately  over- 
lying the  optic  vesicles.  These  placodes  of  thickened  ectoderm 
sink  below  the  general  level  of  the  surface  of  the  head  to  form 
small  vesicles  which  extend  into  the  secondary  optic  vesicles. 
Their  opening  to  the  surface  is  rapidly  constricted  and  even- 
tually they  are  disconnected  altogether  from  the  superficial 
ectoderm.  At  this  stage  the  opening  to  the  outside  still  persists 
although  it  is  very  small  (Fig.  36,  B,  right  eye).  In  sections 
which  do  not  pass  directly  through  the  opening,  the  lens  vesi- 
cle appears  completely  separated  from  the  overlying  ectoderm 
(Fig.  36,  B,  left  eye). 

The  derivation  of  the  lens  from  a  placode  of  thickened  epi- 
thelium which  sinks  below  the  general  surface,  and  eventually 
loses  its  connection  with  the  superficial  ectoderm,  is  strikingly 
similar  to  the  early  steps  in  the  derivation  of  the  auditory 


STRUCTURE   OF   FIFTY-HOUR  CHICKS  99 

vesicle.  But  these  primordia  once  separated  from  the  ectoderm 
follow  divergent  lines  of  differentiation  leading  to  adult  condi- 
tions which  are  structurally  and  functionally  totally  unlike. 
The  origin  of  these  two  structures  from  cell  groups  similarly 
folded  off  from  the  same  germ  layer,  but  which  once  established 
undergo  each  their  own  characteristic  differentiation,  exempli- 
fies a  sequence  of  events  so  characteristic  of  developmental 
processes  in  general  as  to  call  for  at  least  a  comment  in  passing. 

The  Posterior  Part  of  the  Brain  and  the  Cord  Region  of  the 
Neural  Tube. — Caudal  to  the  diencephalon  the  brain  shows  no 
great  change  as  compared  with  the  last  stages  considered.  The 
mesencephalon  is  somewhat  enlarged  and  the  constrictions 
separating  it  from  the  diencephalon  cephalically  and  the 
metencephalon  caudally  are  more  sharply  marked.  The  meten- 
cephalon  is  more  clearly  marked  off  from  the  myelencephalon 
and  its  roof  is  beginning  to  show  thickening.  In  the  myelen- 
cephalon the  neuromeric  constrictions  are  still  evident  in 
the  ventral  and  lateral  walls  (Figs.  34  and  35).  The  dorsal  wall 
has  become  much  thinner  than  the  ventral  and  lateral  walls 
(Fig.  36,  A  and  B)  and  shows  no  trace  of  division  between  the 
neuromeres. 

In  the  cord  region  of  the  neural  tube  the  lateral  walls  have 
become  thickened  at  the  expense  of  the  lumen  so  that  the 
neural  canal  appears  slit-like  in  sections  of  embryos  of  this  age 
(Fig.  36,  £)  rather  than  elliptical  as  it  is  immediately  after 
the  closure  of  the  neural  folds.  At  this  stage  the  closure  of 
the  neural  tube  is  completed  throughout  its  entire  length.  The 
last  regions  to  close  were  at  the  cephaHc  and  caudal  ends  of  the 
neural  groove.  In  younger  stages  where  they  remained  open 
these  regions  were  known  as  the  anterior  neuropore  and  the 
sinus  rhomboidalis,  respectively. 

The  Neural  Crest.— In  the  closure  of  the  neural  tube  the 
superficial  ectoderm  which  at  first  lay  on  either  side  of  the 
neural  groove,  continuous  with  the  neural  plate  ectoderm^ 
becomes  fused  in  the  mid-line  and  separated  from  the  neural 
plate  to  constitute  an  unbroken  ectodermal  covering  (Cf.  Figs. 
17,  Bf  and  28,  B).  At  the  same  time  the  lateral  margins  of  the 
neural  plate  become  fused  to  complete  the  neural  tube.  There 
are  cells  lying  originally  at  the  edges  of  the  neural  folds  which 
are  not  involved  in  the  fusion  of  either  the  superficial  ectoderm 


lOO 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


or  the  neural  plate.  These  cells  form  a  pair  of  longitudinal 
aggregations  extending  one  on  either  side  of  the  mid-dorsal 
line  in  the  angles  between  the  superficial  ectoderm  and  the 
neural  tube  (Fig.  37,  A).  With  the  fusion  of  the  edges  of  the 
neural  folds  to  complete  the  neural  tube,  and  the  fusion  of  the 
superficial  ectoderm  dorsal  to  the  neural  tube,  these  two  longi- 
tudinal cell  masses  become  for  a  time  confluent  in  the  mid-line 


neural  tube 


neural  tube 


Pig.  37. — Drawings  from  transverse  sections  to  show  origin  of  neural  crest 
cells.  The  location  of  the  area  drawn  is  indicated  on  the  small  sketch  to  the 
left  of  each  drawing. 

A,  anterior  rhombencephalic  region  of  30-hour  chick;  B,  posterior  rhomb- 
encephalic  region  of  36-hour  chick;  C,  mid-dorsal  region  of  cord  in  5S-hour 
chick. 


(Fig.  37,  B).  But  because  this  aggregation  of  cells  arises  from 
paired  components  and  soon  again  separates  into  right  and  left 
parts  it  is  to  be  considered  as  potentially  paired.  On  account 
of  its  position  dorsal  to  the  neural  tube  it  is  known  as  the  neural 
crest. 

The  neural  crest  should  not  be  confused  with  the  margin  of 


STRUCTURE    OF   FIFTY-HOUR   CHICKS  lOI 

the  neural  fold  with  which  it  is  associated  before  the  closure 
of  the  neural  tube.  The  margin  of  the  neural  fold  involves 
cells  which  go  into  the  superficial  ectoderm  and  into  the  neural 
tube,  as  well  as  those  which  are  concerned  in  the  formation  of 
the  neural  crest. 

When  first  established  the  neural  crest  is  continuous  antero- 
posteriorly.  As  development  proceeds,  the  cells  of  the  neural 
crest  migrate  ventro-laterally  on  either  side  of  the  spinal  cord 
(Fig.  37,  C),  and  at  the  same  time  become  segmen tally  clus- 
tered. The  segmentally  arranged  cell  groups  thus  derived  from 
the  neural  crest  give  rise  to  the  dorsal  root  ganglia  of  the  spinal 
nerves,  and  in  the  head  region  to  the  ganglia  of  the  sensory 
cranial  nerves.  (For  a  later  stage  of  the  dorsal  root  ganglia  see 
Figure  44.) 

in.  The  Digestive  Tract 

The  Fore-gut. — The  manner  in  which  the  three  primary 
regions  of  the  gut-tract  are  estabUshed  has  already  been  con- 
sidered in  a  general  way  (see  Chapter  XI  and  Fig.  31).  In 
50  to  55-hour  chicks  the  fore-gut  has  acquired  considerable 
length.  It  extends  from  the  anterior  intestinal  portal  cephalad 
almost  to  the  infundibulum  (Fig.  35). 

As  the  first  region  of  the  tract  to  be  established,  the  fore-gut 
is  naturally  the  most  advanced  in  differentiation.  We  can 
already  recognize  a  pharyngeal  and  an  oesophageal  portion. 
The  pharyngeal  region  lies  ventral  to  the  myelencephalon  and 
is  encircled  by  the  aortic  arches  (Fig.  35).  The  pharynx  is 
somewhat  flattened  dorso-ventrally  and  has  a  considerably 
larger  lumen  than  the  oesophageal  part  of  the  fore-gut  (Cf .  Fig. 
36,  B  and  C). 

The  Stomodaeum.^There  is  at  this  stage  no  mouth  opening 
into  the  pharynx.  However,  the  location  where  the  opening 
will  be  formed  is  indicated  by  the  approximation  of  a  ventral 
outpocketing  near  the  anterior  end  of  the  pharynx,  to  a  depres- 
sion formed  in  the  adjacent  ectoderm  of  the  ventral  surface  of 
the  head  (Fig.  35).  The  ectodermal  depression,  known  as  the 
stomodaeum,  deepens  until  its  floor  lies  in  contact  with  the  ento- 
derm of  the  pharyngeal  out-pocketing  (Fig.  35).  The  thin 
layer  of  tissue  formed  by  the  apposition  of  the  stomodaeal  ecto- 
derm to  the  pharyngeal  entoderm  is  known  as  the  oral  plate. 


I02  EARLY   EMBRYOLOGY   OF   THE   CHICK 

Later  in  development  the  oral  plate  breaks  thiough  bringing 
the  stomodaeum  and  the  pharynx  into  open  communication. 
Growth  of  surrounding  structures  deepens  the  original  stomodaeal 
depression,  and  it  becomes  the  oral  cavity.  The  region  of  the 
oral  plate  in  the  embryo  becomes,  in  the  adult,  the  region  of 
transition  from  oral  cavity  to  pharynx. 

The  Pre-oral  Gut. — It  will  be  noted  by  reference  to  Figure 
35  that  the  oral  opening  is  not  established  at  the  extreme 
cephalic  end  of  the  pharynx.  The  part  of  the  pharynx  which 
extends  cephalic  to  the  mouth  opening  is  known  as  the  pre-oral 
gut.  After  the  rupture  of  the  oral  plate,  the  pre-oral  gut 
eventually  disappears,  but  an  indication  of  it  persists  for  a  time 
as  a  small  diverticulum  termed  SeesselFs  pocket(Cf.Figs.  35 
and  43). 

The  Mid-gut. — Although  the  mid-gut  is  still  the  most  ex- 
tensive of  the  three  primary  divisions  of  the  digestive  tract, 
it  presents  little  of  interest.  It  is  nothing  more  than  a  region 
where  the  gut  still  lies  open  to  the  yolk.  It  does  not  have 
even  a  fixed  identity.  As  fast  as  any  part  of  the  mid-gut 
acquires  a  ventral  wall  by  the  closing-in  process  involved  in 
the  progress  of  the  subcephalic  and  subcaudal  folds  it  ceases  to 
be  mid-gut  and  becomes  fore-gut  or  hind-gut.  Differentiation 
and  local  specializations  appear  in  the  digestive  tract  only  in 
regions  which  have  ceased  to  be  mid-gut. 

The  Hind-gut. — The  hind-gut  first  appears  in  embryos  of 
about  55  hours  (Fig.  35).  The  method  of  its  formation  is 
similar  to  that  by  which  the  fore-gut  was  estabhshed.  The 
sub-caudal  fold  undercuts  the  tail  region  and  walls  off  a  gut 
pocket.  The  hind-gut  is  lengthened  at  the  expense  of  the 
mid-gut  as  the  sub-caudal  fold  progresses  cephalad  and  is 
also  lengthened  by  its  own  growth  caudad.  It  shows  no  local 
specializations  until  later  in  development. 

IV.  The  Visceral  Clefts  and  Visceral  Arches 

At  this  stage  the  chick  embryo  has  unmistakable  visceral 
arches  and  visceral  clefts.  Although  only  transitory,  they  are 
morphologically  of  great  importance  not  only  from  the  com- 
parative view  point,  and  because  of  their  significance  as  struc- 
tures exemplifying  recapitulation,   but  also  because  of  their 


STRUCTURE    OF   FIFTY-HOUR   CHICKS  103 

participation  in  the  formation  of  the  embryonic  arterial  system, 
of  some  of  the  ductless  glands,  of  the  eustachian  tube,  and  of 
the  face  and  jaws. 

The  visceral  clefts  are  formed  by  the  meeting  of  ectodermal 
depressions,  the  visceral  furrows,  with  diverticula  from  the 
lateral  walls  of  the  pharynx,  the  pharyngeal  pouches.  During 
most  of  the  time  the  visceral  furrows  are  conspicuous  features 
in  entire  embryos,  they  may  be  seen  in  sections  to  be  closed  by 
a  thin  double  layer  of  tissue  composed  of  the  ectoderm  of  the 
floor  of  the  visceral  furrow  and  the  entoderm  at  the  distal  ex- 
tremity of  the  pharyngeal  pouch  (Fig.  36,  A).  The  breaking 
through  of  this  thin  double  layer  of  tissue  brings  the  pharyngeal 
pouches  into  communication  with  the  visceral  furrows  thereby 
establishing  open  visceral  clefts.  In  birds  an  open  condition  of 
the  clefts  is  transitory.  In  the  chick  the  most  posterior  of  the 
series  of  clefts  never  becomes  open.  Although  some  of  the 
clefts  never  become  open  and  others  open  for  but  a  short  time 
the  term  cleft  is  usually  used  to  designate  these  structures  which 
are  potentially  clefts,  whether  open  or  not. 

The  position  of  the  visceral  clefts  is  best  seen  in  entire  em- 
bryos. They  are  commonly  designated  by  number  beginning 
with  the  first  cleft  posterior  to  the  mouth  and  proceeding 
caudad.  The  first  post-oral  cleft  appears  earliest  in  develop- 
ment and  is  discernible  at  about  46  hours  of  incubation.  Vis- 
ceral cleft  II  appears  soon  after,  and  by  50  to  55  hours  three 
clefts  have  been  formed  (Fig.  34). 

Between  adjacent  visceral  clefts,  the  lateral  body  walls  about 
the  pharynx  are  thickened.  Each  of  these  lateral  thickenings 
in  the  mid-ventral  line  meets  and  merges  with  the  corresponding 
thickening  of  the  opposite  side  of  the  body.  Thus  the  pharynx 
is  encompassed  laterally  and  ventrally  by  a  series  of  arch-like 
thickenings,  the  visceral  or  gill  arches.  The  visceral  arches  like 
the  visceral  clefts  are  designated  by  number,  beginning  at  the 
anterior  end  of  the  styles.  Visceral  arch  I  lies  cephalic  to  the 
first  post-oral  cleft,  between  it  and  the  mouth  region.  Because 
of  the  part  it  plays  in  the  formation  of  the  mandible  it  is  also 
designated  as  the  mandibular  arch.  Visceral  arch  II  is  fre- 
quently termed  the  hyoid  arch,  and  visceral  cleft  I,  because  of 
its  position  between  the  mandibular  and  hyoid  arches,  is  known 
as  the  hyomandibular  cleft.     Posterior  to  the  hyoid  arch  the 


I04  EARLY  EMBRYOLOGY   OF   THE   CHICK 

visceral  arches  and  clefts  are  ordinarily  designated  by  their 
post-oral  numbers  only. 

There  are  other  structures  which  are  just  beginning  to  be 
differentiated  in  the  pharyngeal  region  and  fore-gut  of  embryos 
of  this  stage,  but  it  seems  better  to  consider  them  in  connection 
with  later  stages  when  their  significance  will  be  more  readily 
grasped. 

V.  The  Circulatory  System 

The  Heart. — In  embryos  of  30  to  40  hours  incubation  we 
traced  the  expansion  of  the  heart  till  it  was  bent  to  the  right  of 
the  embryo  In  the  form  of  a  U-shaped  tube  (Figs.  19,  21,  23). 
The  disappearance  of  the  dorsal  mesocardium  except  at  its 
li  posterior  end,  leaves  the  mid-region  of  the  heart  lying  unat- 
'  tached  and  extending  to  the  right,  into  the  pericardial  region  of 
the  coelom.  The  heart  is  fixed  with  reference  to  the  body  of  the 
embryo  at  its  cephalic  end  where  the  ventral  aortic  roots  lie 
embedded  beneath  the  floor  of  the  pharynx,  and  caudally  in  the 
sinus  region  where  it  is  attached  by  the  omphalomesenteric 
veins,  by  the  ducts  of  Cuvier,  and  by  the  persistent  portion  of 
the  dorsal  mesocardium. 

During  the  period  between  30  and  55  hours  of  incubation  the 
heart  itself  is  growing  more  rapidly  than  is  the  body  of  the 
embryo  in  the  region  where  the  heart  lies.  Since  its  cephalic 
and  caudal  ends  are  fixed,  the  unattached  mid-region  of  the 
heart  becomes  at  first  U-shaped  and  then  twisted  on  itself  to 
form  a  loop.  The  atrial  region  of  the  heart  is  forced  somewhat 
to  the  left,  and  the  conus  region  is  thrown  across  the  atrial 
region  by  being  twisted  to  the  right  and  dorsally.  The  ven- 
tricular region  constitutes  the  loop  proper  (Cf.  Figs.  22,  29  and 
34).  This  twisting  process  reverses  the  original  cephalo- 
caudal  relations  of  the  atrial  and  ventricular  regions.  Before 
the  twisting,  the  atrial  region  of  the  heart  was  caudal  to  the 
ventricular  region  as  it  is  in  the  adult  fish  heart.  In  the  twist- 
ing of  the  heart  the  atrial  region,  by  reason  of  its  association 
with  the  fixed  sinus  region  of  the  heart,  undergoes  relatively 
little  change  in  position.  The  ventricular  region  is  carried,  over 
the  dextral  side  of  the  atrium  and  comes  to  lie  caudal  to  it,  thus 
arriving  in  the  relative  position  it  occupies  in  the  adult  heart. 
The  bending  and  subsequent  twisting  of  the  heart  lead  toward 


STRUCTURE   OF  FIFTY-HOUR   CHICKS  IO5 

its  division  into  separate  chambers.  As  yet,  however,  no  indi- 
cation of  the  actual  partitioning  off  of  the  heart  is  apparent.  It 
is  still  essentially  a  tubular  organ  through  which  the  blood  passes 
directly  without  any  division  into  separate  channels  or  currents. 

The  Aortic  Arches. — In  33  to  38  hour  chicks  the  ventral 
aortae  communicate  with  the  dorsal  aortae  over  a  single  pair  of 
aortic  arches  which  bend  around  the  anterior  end  of  the  pharynx 
(Figs.  23  and  24) .  With  the  formation  of  the  visceral  arches  new 
aortic  arches  appear.  The  original  pair  of  aortic  arches  comes 
to  lie  in  the  mandibular  arch,  and  the  new  aortic  arches  are 
formed  caudal  to  the  first  pair,  one  pair  in  each  visceral  arch. 
In  chicks  of  50  to  55  hours,  three  pairs  of  aortic  arches  have  been 
established  and  a  fourth  is  usually  beginning  to  form  (Figs. 
34,  35,  and  36,  A  and  5). 

The  Fusion  of  the  Dorsal  Aortae. — The  dorsal  aortae  arise  as 
vessels  paired  throughout  their  entire  length  (Fig.  23).  As 
development  progresses  they  fuse  in  the  mid-line  to  form  the 
unpaired  dorsal  aorta  familiar  in  adult  anatomy.  This  fusion 
takes  place  first  at  about  the  level  of  the  sinus  venosus  and 
progresses  thence  cephalad  and  caudad.  Cephalically  it  never 
extends  to  the  pharyngeal  region.  Caudally  the  whole  length 
of  the  aorta  is  eventually  involved.  At  this  stage  the  fusion 
has  progressed  caudad  to  about  the  level  of  the  14th  somite 
(Figs.  34,  35,  36). 

The  Cardinal  and  Omphalomesenteric  Vessels. — The  rela- 
tionships of  the  cardinal  veins  and  the  omphalomesenteric 
vessels  are  little  changed  from  the  conditions  in  40  to  50  hour 
chicks.  The  posterior  cardinals  have  elongated,  keeping  pace 
with  the  caudal  progress  of  differentiation  in  the  mesoderm. 
They  lie  just  dorsal  to  the  intermediate  mesoderm  in  the  angle 
formed  between  it  and  the  somites  (Fig.  36,  D).  The  entrance 
of  the  omphalomesenteric  veins  into  the  sinus  venosus,  and  the 
origin  of  the  omphalomesenteric  arteries  from  the  dorsal  aortae 
show  little  change  from  conditions  familiar  from  the  study  of 
younger  embryos. 

VI.  The  Differentiation  of  the  Somites 

When  the  somites  are  first  formed  they  consist  of  a 
nearly  solid  mass  of  cells  derived  from  the  dorsal  mesoderm  (Fig. 
sSj  A).     The  cells  composing  them  show  a  more  or  less  radial 


io6 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


neural  fold 

ectoderm  of  head 


somite 

intermediate  mesoderm 

somatic  mesoderm 
coelom 
splanchnic  mesoderm 
entoderm 


epithelial  layer  of  somite 

core  of  somite 

pronephric  tubule 
(intermediate  mesoderm) 

somatic  mesoderm 

coelom 
iplanchnic  mesoderm 
entoderm 


D 


epithelial  layer  of  somite 

cavity  of  somite 
core  of  somite 
migrating  cells 

posterior  cardinal  vein 
mesonephric  duct 
mesonephric  tubule 
coelom 
dorsal  aorta 


dorsal  ganglion 

(neural  crest) 

myotome 

dermatome 
sclerotome 

myocoele 

posterior  cardinal  vein 

mesonephric  duct 
mesonephric  tubule 

dorsal  aorta 

intra-embryonic  coelom 

extra-embryonic  coelom 


Pig.  38. — Drawings  from  transverse  sections  to  show  the  differentiation  of  the 

somites. 
A,  second  somite  of  4-somite  chick;  B,  ninth  somite  of  12-somite  chick;  C, 
twentieth  somite  of  30-somite  chick;  D,  seventeenth  somite  of  33-somite  chick. 


STRUCTURE    OF   FIFTY-HOUR   CHICKS  107 

arrangement.  In  the  center  of  the  somite  a  cavity  is  usually 
discernible.  This  cavity  is  at  first  extremely  minute.  In 
somites  which  have  been  recently  formed  it  may  be  altogether 
wanting. 

As  the  somite  becomes  more  sharply  marked  ofif  the  radial 
arrangement  of  the  outer  zone  of  cells  appears  more  definitely 
(Fig.  38,  B).  The  boundaries  of  the  central  cavity  are  con- 
siderably extended  but  its  lumen  is  almost  completely  filled  by 
a  core  of  irregularly  arranged  cells.  In  sections  which  pass 
through  the  middle  of  the  somite,  this  central  core  of  cells  is 
seen  to  arise  from  the  lateral  wall  of  the  somite  where  it  is 
continuous  with  the  intermediate  mesoderm. 

A  little  later  in  development  the  outer  zone  of  cells  on  the 
ventro-mesial  face  of  the  somite  loses  its  originally  definite 
boundaries  and  becomes  merged  with  the  central  core  of  cells. 
This  ill-defined  cell  aggregation,  known  as  the  sclerotome,  be- 
comes mesenchymal  in  characteristics,  and  extends  ventro- 
mesiad  from  the  somite  of  either  side  toward  the  notochord 
(Fig.  2)^,  C  and  D).  The  cells  of  the  sclerotomes  of  either  side 
continue  to  converge  about  the  notochord  and  later  take  part 
in  the  formation  of  the  axial  skeleton. 

Duting  the  formation  of  the  sclerotome  the  dorsal  part  of 
the  original  outer  cell-zone  of  the  somite  has  maintained  its 
definite  boundaries  and  epithehal  characteristics.  The  part  of 
this  outer  zone  which  lies  parallel  to  the  ectoderm  is  known  as 
the  dermatome  (Fig.  38,  C  and  D).  It  later  becomes  asso- 
ciated with  the  ectoderm  and  forms  the  deeper  layers  of  the 
integument,  the  ectoderm  giving  rise  to  the  epithelial  layer 
only. 

The  dorso-mesial  portion  of  the  outer  zone  of  the  somite  be- 
comes the  myotome.  It  is  folded  somewhat  laterad  from  its 
original  position  next  to  the  neural  tube  (Fig.  2>^,  C)  and  comes 
to  lie  ventro-mesial  to  the  dermatome  and  parallel  to  it  (Fig. 
38,  D).  (A  later  stage  in  the  differentiation  of  the  somite  is 
shown  in  Figure  44) .  The  portion  of  the  original  cavity  which 
persists  for  a  time  between  the  dermatome  and  myotome 
is  termed  the  myocoele.  The  myotomes  undergo  the  most 
extensive  growth  of  any  of  the  parts  of  the  somite,  giv- 
ing rise  eventually  to  the  entire  skeletal  musculature  of  the 
body. 


Io8  EARLY   EMBRYOLOGY   OF   THE   CHICK 

VII.  The  Urinary  System 

In  the  section-diagrams  of  Figure  36,  Z)  and  E,  certain  parts 
of  the  urinary  system  which  have  been  established  in  chicks  of 
50  to  55  hours  will  be  found  located  and  labeled.  The  urinary 
system  is  relatively  late  in  becoming- differentiated.  Only  a 
few  of  the  early  steps  in  its  formation  can  at  this  time  be  made 
out.  Many  structures  which  later  become  of  great  importance 
are  not  represented  even  by  primordial  cell  aggregations.  Ex- 
cept for  those  well  grounded  in  comparative  anatomy,  any 
logical  discussion  of  the  structures  which  have  appeared  must 
anticipate  much  that  occurs  later  in  development.  Consider- 
ation of  the  mode  of  origin  and  significance  of  the  nephric 
organs  appearing  at  this  stage  has,  therefore,  been  deferred. 


CHAPTER  XIII 

THE    DEVELOPMENT    OF    THE    CHICK    DURING    THE 
THIRD  AND  FOURTH  DAYS  OF  INCUBATION 

1.  External  Features. 

Torsion;  flexion;  the  visceral  arches  and  clefts;  the  oral 
region;  the  appendage  buds;  the  allantois. 
II.  The  Nervous  System. 

Summary  of  development  prior  to  the  third  day;  the 
formation  of  the  telencephaHc  vesicles;  the  diencepha- 
lon;  the  mesencephalon;  the  metencephalon;  the 
myelencephalon;  the  gangUa  of  the  cranial  nerves; 
the  spinal  cord;  the  spinal  nerve  roots. 

III.  The  Sense  Organs. 

The  eye;  the  ear;  the  olfactory  organs. 

IV.  The  Digestive  and  Respiratory  Systems. 

Summary  of  development  prior  to  the  third  day;  the 
establishment  of  the  oral  opening;  the  pharyngeal 
derivatives;  the  trachea;  the  lung-buds;  the  oesopha- 
gus and  stomach;  the  liver;  the  pancreas;  the  mid- 
gut region;  the  cloaca;  the  proctodaeum  and  the  cloa- 
cal  membrane. 
V.  The  Circulatory  System. 

The  functional  significance  of  the  embryonic  circulation; 
the  vitelHne  circulation;  the  allantoic  circulation;  the 
intra-embryonic  circulation;  the  heart. 
VI.  The  Urinary  System. 

The  general  relationships  of  pronephros,  mesonephros, 
and  metanephros;  the  pronephric  tubules  of  the  chick; 
the  mesonephric  tubules. 
VII.  The  Coelom  and  Mesenteries. 

I.  External  Features 

Torsion. — Chicks  of  three  days  incubation  (Fig.  39)  have 
been  affected  by  torsion  throughout  their  entire  length.  Tor- 
sion is  complete  well  posterior  to  the  level  of  the  heart  but 

109 


no 


EARLY   EMBRYOLOGY    OF    THE    CHICK 


the  caudal  portion  of  the  embryo  is  not  yet  completely  turned 
on  its  side.  In  four-day  chicks  the  entire  body  has  been 
turned  through  90  degrees  and  the  embryo  lies  with  its  left  side 
on  the  yolk  (Fig.  40). 


0  myelencephalon 

ganglion  IX 
visceral  cleft  II 

aortic  arch  IV 


bulbo-conus 
arteriosus 


hyoid  arch 
auditory  vesicle     /  .  hyomandibular  cleft 

mandibular  arch 
ganglion  V 

metencephalon 


ant.  cardinal  v. 


mesencephalon 


horoid   fissure 
—  lens 

sensory  layer 
pigment  layer 


appendage  bud 


posterior 
appendage  bud 


vitelline  artery 


Pig.  39. 


-Dextro-dorsal  view   (  X  14)   of  entire  chick  embryo  of  36   somites 
(about  three  days  incubation). 


Flexion. — The  cranial  and  cervical  flexures  which  appeared 
in  embryos  during  the  second  day  have  increased  so  that  in 
three-day  and  four-day  chicks  the  long  axis  of  the  embryo  shows 
nearly  right-angled  bends  in  the  mid-brain  and  in  the  neck 
region.  The  mid-body  region  of  three-day  chicks  is  slightly 
concaved  dorsally.  This  is  due  to  the  fact  that  the  embryo 
is  still  broadly  attached  to  the  yolk  in  that  region.  By  the 
end  of  the  fourth  day  the  body  folds  have  undercut  the  embryo 
so  it  remains  attached  to  the  yolk  only  by  a  slender  stalk. 
The  yolk-stalk  soon  becomes  elongated  allowing  the  embryo  to 
become  first  straight  in  the  mid-dorsal  region,  and  then  convex 


STRUCTURE    OF    FOUR-DAY   CHICKS 


III 


dorsally.  At  the  same  time  the  caudal  flexure  is  becoming  more 
pronounced.  The  progressive  increase  in  the  cranial,  cervical, 
dorsal,  and  caudal  flexures  results  in  the  bending  of  the  embryo 
on  itself  so  that  its  originally  straight  long-axis  becomes 
C-shaped  and  its  head  and  tail  lie  close  together  (Fig.  40). 


myelencephalon 
visceral  arch  III 
bulbo-conusarteriosus 
atrium 


auditory  vesicle 

endolymphatic  duct 
ganglion  IX/  /  ganglion  VII-VIII 


hyomandi  bular  cleft 
mandibular  arch 

ganglion  V 


meten- 
cephalon 


mesen- 
cephalon 


anterior 
appendage  bud 

omphalo- 
mesenteric 
vein 


border 
mesoneph; 


posterior  appendage  bud 


Fig.  40. — Dextral  view  of  entire  chick  embryo  of  41  somites  (about  four  days 

incubation) . 

The  Visceral  Arches  and  Clefts. — A  fourth  visceral  cleft  has 
appeared  caudal  to  the  three  that  were  already  formed  in  55- 
hour  chicks.  The  visceral  arches  are  thicker  and  more  conspicu- 
ous than  in  earlier  embryos.  In  lightly  stained  whole-mounts 
of  a  three-day  chick  it  is  still  possible  to  make  out  the  aortic 
arches  running  through  the  visceral  arches.  In  a  chick  of  four 
days  the  visceral  arches  have  become  so  much  thickened  that  it 
is  very  difficult  to  see  the  vessels  traversing  them. 

The  Oral  Region. — The  cervical  flexure  presses  the  pharyn- 
geal region  and  the  ventral  surface  of  the  head  so  closely  to- 
gether that  it  is  difficult  to  make  out  the  topography  of  the  oral 


112 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


region  by  study  of  entire  embryos.  If  the  head  and  pharyngeal 
region  are  cut  from  the  trunk  and  viewed  from  the  ventral 
aspect  the  relations  of  the  structures  about  the  mouth  are  well 
shown  (Fig.  41).  The  mandibular  arch  forms  the  caudal 
boundary  of  the  oral  depression.  Arising  on  either  side  in 
connection  with  the  mandibular  arch  are  paired  elevations,  the 
maxillary  processes,  which  grow  mesiad  and  form  the  cephalo- 
lateral  boundaries  of  the  mouth  opening.  The  nasal  pits 
appear  as  shallow  depressions  in  the  ectoderm  of  the  anterior 
part  of  the  head  which  overhangs  the  mouth  region.     Surround- 


epiphytif 


lateral  telencephalic 
vesicle 


Pig.  41. — Drawing  to  show  the  external  appearance  of  the  structures  in  the  oral 
region  of  a  four-day  chick.     Ventral  aspect. 


ing  each  nasal  pit  is  a  U-shaped  elevation  with  its  limbs  directed 
toward  the  oral  cavity.  The  lateral  limb  of  the  elevation  is  the 
naso-lateral  process,  and  the  median  limb  is  the  naso-medial 
process.  As  development  proceeds  the  two  naso-medial  proces- 
ses grow  toward  the  mouth  and  meet  the  maxillary  pro- 
cesses which  are  growing  in  from  either  side.  The  fusion  of 
the  two  naso-medial  processes  with  each  other  in  the  mid-line, 
and  the  fusion  of  each  of  them  laterally  with  the  maxillary 
process  of  its  own  side  gives  rise  to  the  upper  jaw  (maxilla). 
The  fusion  in  the  mid-line  of  the  right  and  left  components  of 
the  mandibular  arch  gives  rise  to  the  lower  jaw  (mandible). 

The  Appendage  Buds. — Both  the  anterior  and  posterior  ap- 
pendage-buds have  appeared  in  embryos  of  three  days.     They 


STRUCTURE    OF    FOUR-DAY   CHICKS  II3 

are  formed  by  bud-like  outgrowths  from  somites.  The  anterior 
appendages  arise  opposite  somites  17  to  19  inclusive,  and  the 
posterior  appendages  arise  opposite  somites  26  to  32  inclusive. 
During  the  fourth  day  the  appendage  buds  increase  rapidly  in 
size  and  become  elongated  but  otherwise  their  appearance  and 
their  relationships  show  little  change. 

The  Allantois. — The  development  of  the  extra-embryonic 
membranes  has  already  been  considered  (Chap.  XI)  and  needs 
no  further  discussion  here.  In  order  to  show  the  embryos  more 
clearly,  the  extra-embryonic  membranes,  except  for  the  allan- 
tois, have  been  removed  from  the  specimens  drawn  in  Figures 
39  and  40.  The  cut  edge  of  the  amnion  shows  at  its  anterior 
attachment  to  the  body,  opposite  the  anterior  appendage  bud 
and  just  caudal  to  the  tip  of  the  ventricle.  The  allantois  in 
the  three-day  chick  is  as  yet  small  and  is  concealed  by  the  pos- 
terior appendage  buds.  In  four-day  embryos  it  has  undergone 
rapid  enlargement  and  projects  from  the  umbilical  region  as  a 
stalked  vesicle  of  considerable  size. 

II.  The  Nervous  System 

Simmiary  of  Development  Prior  to  the  Third  Day. — The 

earliest  indication  of  the  formation  of  the  central  nervous  sys- 
tem appears  in  chicks  of  16  to  18  hours  as  a  local  thickening  of 
the  ectoderm  which  forms  the  neural  plate  (Fig.  11).  The 
neural  plate  then  becomes  longitudinally  folded  to  form  the 
neural  groove  (Figs.  14  and  15).  By  fusion  of  the  margins  of 
the  neural  folds,  first  in  the  cephalic  region  and  later  caudally, 
the  neural  groove  is  closed  to  form  a  tube  and  at  the  same  time 
separated  from  the  body  ectoderm.  The  cephalic  portion  of 
the  neural  tube  becomes  dilated  to  form  the  brain  and  the  re- 
mainder of  the  neural  tube  gives  rise  to  the  spinal  cord  (Figs. 
18  and  21). 

In  its  early  stages  the  brain  shows  a  series  of  enlargements 
in  its  ventral  and  lateral  walls,  indicative  of  its  fundamental 
metameric  structure.  In  the  establishment  of  the  three  vesicle 
condition  of  the  brain,  the  lines  of  demarcation  between  pros- 
encephalon, mesencephalon,  and  rhombencephalon  are  formed 
by  the  exaggeration  of  certain  of  the  inter-neuromeric  constric- 
tions and  the  obliteration  of  others  (see  Chap.  IX  and  Fig.  20). 


114  EARLY   EMBRYOLOGY   OF   THE   CHICK 

The  original  neuromeric  enlargements  persist  longest  in  the 
rhombencephalon. 

The  three-vesicle  condition  of  the  brain  is  transitory.  By 
forty  hours  the  division  of  the  rhombencephalon  into  meten- 
cephalon  and  myelencephalon  is  clearly  indicated  (Figs.  20,  D 
and  22).  The  division  of  the  prosencephalon  and  the  estabhsh- 
ment  of  the  five-vesicle  condition  characteristic  of  the  adult 
brain,  does  not  take  place  until  somewhat  later. 

In  chicks  of  55  hours  (Figs.  34  and  35)  the  appearance  of  the 
cranial  flexure  has  resulted  in  the  bending  of  the  brain  so  that 
the  entire  prosencephalon  is  displaced  ventrad  and  then  toward 
the  heart.  At  the  same  time  the  head  of  the  embryo  has  under- 
gone torsion  and  lies  with  its  left  side  on  the  yolk.  Although 
flexion  and  torsion  have  thus  completely  changed  the  general 
appearance  of  the  brain  as  seen  in  entire  embryos,  the  regions 
already  established  in  40-hour  chicks  are  still  evident.  The 
prosencephalon  has,  however,  become  very  noticeably  enlarged 
cephalic  to  the  optic  vesicles,  and  a  slight  constriction  in  its 
dorsal  wall  indicates  the  beginning  of  the  demarcation  of  the 
telencephalic  region  from  the  diencephalic  region. 

The  Formation  of  the  Telencephalic  Vesicles. — By  the  end 
of  the  third  day  the  antero-lateral  walls  of  the  primary  fore- 
brain  have  been  evaginated  to  form  a  pair  of  vesicles  lying  one 
on  either  side  of  the  mid-line  (Figs.  39,  41,  and  42,  B).  These 
lateral  evaginations  are  known  as  the  telencephalic  vesicles. 
The  openings  through  which  their  cavities  are  continuous  with 
the  lumen  of  the  median  portion  of  the  brain  are  later  known 
as  the  foramina  of  Monro.  The  telencephahc  division  of 
the  brain  includes  not  only  the  two  lateral  vesicles  but  also 
the  median  portion  of  the  brain  from  which  they  arise.  The 
teloccele  has  therefore  three  divisions,  a  median,  broadly  con- 
fluent posteriorly  with  the  diocoele,  and  two  lateral,  connecting 
with  the  median  through  the  foramina  of  Monro  (Fig.  42,  C). 

Before  the  formation  of  the  telencephalic  vesicles  the  most 
anterior  part  of  the  brain  lay  in  the  mid-line,  but  the  rapid 
growth  of  the  telencephalic  vesicles  soon  carries  them  anteriorly 
beyond  the  median  portion  of  the  teloccele.  The  median  ante- 
rior wall  of  the  teloccele  which  formerly  was  the  most  anterior 
part  of  the  brain,  and  which  remains  the  most  anterior  part  of 
the  brain  lying  in  the  mid-line,  is  known  as  the  lamina  terminalis 


STRUCTURE    OF   FOUR-DAY   CHICKS 


"5 


(Figs.  42,  A,  and  C,  and  43).  The  telencephalic  vesicles  become 
the  cerebral  hemispheres,  and  their  cavities  become  the  paired 
lateral  ventricles  of  the  adult  brain.  The  hemispheres  undergo 
enormous  enlargement  in  their  later  development  and  extend 
dorsally  and  posteriorly  as  well  as  anteriorly,  eventually  cover- 
ing the  entire  diencephalon  and  mesencephalon  under  their 
posterior  lobes. 


metacoele 
(  ventricle  IV  ) 
thin  roof  of  myelencephalon 
myelocoele 


cle  IV  ) 


ventral  cephalic  fold 


spinal  cord 


recessus  opticus 
lamina  termina 

median  telocoele 
(ventricle  III) 
recessus   neuroporicus 


meso-metenceohalic  fold 


mesocoele 
(Sylvian  aqueduct  j 

location  of 
posterior  comm  issure 
mescKliencephalic   fold 
tuberculum  posterius 
diocoele( ventricle  III  ) 
epiphysis 
velum  transversum 


metencephalon 


mesencephalon 


gangli 
ganglion  VII  VIII 


lamina  .. 

terminalis  /median  telocoele 

( ventricle  III  ) 

foramen  of  Monro 


(sylvian  aqueduct^ 


lateral  telencephalic 
vesicle 


metacoele 
^ventricle    IV ) 

myelocoele 
(  ventricle  IV) 

position  of 
auditory  vesicle 

spinal  cord 


Fig.  42. — Diagrams  to  show  the  topography  of  the  brain  of  a  four-day  chick. 
A,  plan  of  sagittal  section.  The  arbitrary  boundaries  between  the  various 
brain  vesicles  (according  to  von  Kupffer)  are  indicated  by  broken  lines.  B, 
dextral  view  of  a  brain  which  has  been  dissected  free.  C,  schematic  frontal 
section  plan  of  brain.  The  flexures  of  the  brain  are  supposed  to  have  been 
straightened  before  the  section  was  cut. 

As  a  matter  of  convenience  in  dealing  with  the  morphology 
of  the  brain,  more  or  less  arbitrary  lines  of  division  between 
the  adjacent  brain  regions  are  recognized.  The  division  be- 
tween telencephalon  and  diencephalon  is  an  imaginary  line 
drawn  from  the  velum  transversum  to  the  recessus  opticus 


ii6 


EARLY   EMBRYOLOGY    OF    THE    CHICK 


(Fig.  42,  A).  Velum  transversum  is  the  name  given  to  the 
internal  ridge  formed  by  the  deepening  of  the  dorsal  constriction 
which  was  first  noted  in  chicks  of  55  hours  as  indicating  the 
impending  division  of  the  primary  fore-brain  (Fig.  35).  The 
recessus  opticus  is  a  transverse  furrow  in  the  floor  of  the  brain 
which  in  the  embryo  leads  on  either  side  into  the  lumina  of  thp 
optic  stalks. 

The  Diencephalon. — The  lateral  walls  of  the  diencephalon  at 
this  stage  show  little  differentiation  except  ventrally  where  the 


mandibular  arch 

Seetiell's  pocket 

Rathke's  pocket 


.^>^ 


omph.  met, 
vein 


tneionephros 
somite 


dortal  aorta 


tuberculum 
posteriuB 
infundibulum 


allantoic  vesicle 


somite 
allantoic  stallr 


proctodaeum 
post- anal  gut 
cloaca 


—  splanchnopleure 
of  yolk  sac 


Fig.  43.  — Diagram  of  median  longitudinal  section  of  four-day  chick.  Due 
to  a  slight  bend  in  the  embryo  the  section  is  para-sagittal  in  the  mid-dorsal 
region  but  for  the  most  part  it  passes  through  the  embryo  in  the  sagittal  plane. 

optic  stalks  merge  into  the  walls  of  the  brain.  The  develop- 
ment of  the  epiphysis  as  a  median  evagination  in  the  roof  of  the 
diencephalon  has  already  been  mentioned  (Chap.  XII).  Ex- 
cept for  some  elongation  it  does  not  differ  from  its  condition 
when  first  formed  in  embryos  of  about  55  hours.  The  in- 
fundibular depression  in  the  floor  of  the  diencephalon  has  be- 


STRUCTURE  OF  FOUR-DAY  CHICKS  II7 

come  appreciably  deepened  and  lies  in  close  proximity  to 
Rathke's  pocket  with  which  it  is  destined  to  fuse  in  the  forma- 
tion of  the  hypophysis  (Fig.  43).  Later  in  development  the 
lateral  walls  of  the  diencephalon  become  greatly  thickened  to 
form  the  thalami,  thus  reducing  the  size  and  changing  the 
shape  of  the  diocoele,  which  is  known  in  adult  anatomy  as  the 
third  brain  ventricle.  The  anterior  part  of  the  roof  of  the 
diencephalon  remains  thin  and  by  the  ingrowth  of  blood  vessels 
from  above  is.  pushed  into  the  third  ventricle  to  form  the  an- 
terior choroid  plexus. 

The  boundary  between  the  diencephalon  and  the  mesen- 
cephalon is  an  imaginary  line  drawn  from  the  internal  ridge 
formed  by  the  original  dorsal  constriction  between  the  primary 
fore-brain  and  mid-brain,  to  the  tuberculum  posterius  (Fig. 
42,  A).  The  tuberculum  posterius  is  a  rounded  elevation  in 
the  floor  of  the  brain  of  importance  chiefly  because  it  is  regarded 
as  marking  the  boundary  between  diencephalon  and  mesen- 
cephalon. 

The  Mesencephalon.— The  mesencephalon  as  yet  shows  no 
specializations,  beyond  a  thickening  of  its  walls.  The  dorsal 
and  lateral  walls  of  the  mesencephalon  later  increase  rapidly 
in  thickness  and  become  the  optic  lobes  (corpora  quadrigemina) 
of  the  adult  brain.  The  optic  lobes  should  not  be  confused  with 
the  optic  vesicles  arising  from  the  diencephalon  of  the  embryo. 
They  are  entirely  different  structures.  The  floor  of  the  mesen- 
cephalon also  becomes  greatly  thickened  and  is  known  in  the 
adult  as  the  crura  cerebri.  It  serves  as  the  main  pathway  of  the 
fiber  tracts  which  connect  the  cerebral  hemispheres  with  the 
posterior  part  of  the  brain  and  the  spinal  cord.  The  originally 
capacious  mesocoele  is  thus  reduced  by  the  thickening  of  the 
walls  about  it  to  a  narrow  canal  (Aqueduct  of  Sylvius). 

The  Metencephalon. — The  boundary  between  the  mesen- 
cephalon and  metencephalon  is  indicated  by  the  original  inter- 
neuromeric  constriction  which  separated  them  at  the  time^of 
their  estabHshment  (Cf.  Figs.  20  and  42).  The  caudal  boun- 
dary of  the  metencephalon  is  not  definitely  defined.  It  is 
regarded  as  being  located  approximately  at  the  point  where 
the  brain  roof  changes  from  the  thickened  condition  character- 
istic of  the  metencephalon  to  the  thin  condition  characteristic 
of  the  myelencephalon.     The  metencephalon  shows  practically 


Il8  EARLY   EMBRYOLOGY    OF    THE    CHICK 

no  differentiation  in  four-day  chicks.  Later  in  development 
there  is  ventrally  and  laterally  an  extensive  ingrowth  of  fiber 
tracts  giving  rise  to  the  pons  and  to  the  cerebellar  peduncles 
of  the  adult  metencephalon.  The  roof  of  the  metencephalon 
undergoes  extensive  enlargement  and  becomes  the  cerebellum 
of  the  adult  brain. 

The  Myelencephalon. — In  the  myelencephalon  the  dorsal 
wall  has  become  greatly  reduced  in  thickness  indicative  of  its 
final  fate  as  the  thin  roof  of  the  medulla.  Like  the  roof  of  the 
diencephalon,  the  roof  of  the  myelencephalon  later  receives  a 
rich  supply  of  small  blood  vessels  by  which  it  is  pushed  into 
the  myelocoele  to  form  the  posterior  choroid  plexus  (choroid 
plexus  of  the  fourth  ventricle).  The  ventral  and  lateral  walls 
of  the  myelencephalon  become  the  floor  and  side-walls  of  the 
medulla  of  the  adult  brain. 

The  Ganglia  of  the  Cranial  Nerves. — In  the  brain  region,  cells 
derived  from  the  cephalic  portion  of  the  neural  crest  have  be- 
come aggregated  to  form  ganglia.  The  largest  and  the  most 
clearly  defined  of  the  gangha  present  in  four-day  chicks  is  the 
Gasserian  ganglion  of  the  fifth  (trigeminal)  cranial  nerve  (Fig. 
42,  B).  It  lies  ventro-laterally,  opposite  the  most  anterior 
neuromere  of  the  myelencephalon.  From  its  cells  sensory 
nerve  fibers  grow  mesiad  into  the  brain  and  distad  to  the  face 
and  mouth  region.  In  four-day  chicks  the  beginning  of  the 
ophthalmic  division  of  the  fifth  nerve  extends  from  the  ganglion 
toward  the  eye,  and  the  beginning  of  the  mandibulo-maxillary 
division  is  growing  toward  the  angle  of  the  mouth  (Fig.  40). 
Immediately  cephahc  to  the  auditory  vesicle  is  a  mass  of  neural 
crest  cells  which  is  the  primordium  of  the  ganglia  of  the  seventh 
and  eighth  nerves.  The  separation  of  this  double  primordium 
to  form  the  geniculate  ganglion  of  the  seventh  nerve  and  the 
acoustic  ganghon  of  the  eighth  nerve  begins  during  the  fourth 
day.  Posterior  to  the  auditory  vesicle  the  ganglion  of  the 
ninth  nerve  can  be  clearly  seen  even  in  whole-mounts  (Fig.  40). 
The  gangha  of  the  tenth  (vagus)  nerves  can  be  recognized  in 
sections  of  chicks  at  the  end  of  the  fourth  day  but  are  difficult 
to  make  out  in  whole-mounts. 

The  Spinal  Cord. — The  spinal  cord  region  of  the  neural  tube 
when  first  established,  exhibits  a  lumen  which  is  elliptical  in 
cross  section.     As  development  progresses  the  lateral  walls  of 


STRUCTURE    OF   FOUR-DAY   CHICKS 


119 


the  cord  become  greatly  thickened  in  contrast  with  the  dorsal 
and  ventral  walls  which  remain  thin.  In  this  process  the  lumen 
(central  canal)  becomes  compressed  laterally  until  it  appears  in 
cross  section  as  little  more  than  a  vertical  slit.  The  thin  dorsal 
wall  of  the  tube  is  known  as  the  roof  plate;  the  thin  ventral 
wall  as  the  floor  plate;  and  the  thickened  side  walls  as  the 
lateral  plates. 

The  Spinal  Nerve  Roots. — During  the  fourth  day  the  estab- 
lishment of  the  spinal  nerve  roots  has  begun.  The  growth  of 
nerve  fibers  from  the  neuroblasts  can  only  be  traced  with  the  aid 
of  special  methods  of  staining.     The  more  general  steps  in  the 


spinal  cord 


dorsal 

ganglion 


dorsal  root 
ventral  root 
spinal  nerve 


neuron  of 
ventral  root 
(motor) 


Pig.  44. — Drawing  to  show  the  structure  and  relations  of  a  spinal  ganglion 
and  the  roots  of  a  spinal  nerve.  The  left  half  of  the  drawing  represents  struc- 
tures as  they  appear  after  treatment  by  the  usual  nuclear  staining  method.  The 
right  half  of  the  section  shows  schematically  the  nerve  cells  and  the  fibers  grow- 
ing out  from  them  as  they  may  be  demonstrated  by  the  Golgi  method.  {Nerve 
cells  and  fibers  after  Ramon  y  Cajdl.) 


development  of  the  roots  of  the  spinal  nerves  can,  however,  be 
followed  in  sections  prepared  by  the  ordinary  methods. 

In  the  adult  each  spinal  nerve  is  connected  with  the  cord  by 
two  roots,  a  dorsal  root  which  is  sensory  in  function  and  a  ven- 
tral root,  which  is  motor  in  function.  Lateral  to  the  cord  the 
dorsal  and  ventral  roots  unite.  The  spinal  ganglion  (dorsal 
root  ganglion)  is  located  on  the  dorsal  root  between  the  spinal 
cord  and  the  point  where  dorsal  and  ventral  roots  unite.  Distal 
to  the  union  of  dorsal  and  ventral  roots  is  a  branch,  the  ramus 


I20  EARLY   EMBRYOLOGY    OF    THE    CHICK 

communicans,  which  extends  ventrad  to  a  ganglion  of  the  sym- 
pathetic nerve  cord. 

When  first  formed  from  the  neural  crest  cells,  the  spinal 
ganglion  has  no  connection  with  the  cord  (Fig.  37).  The  dorsal 
root  is  established  by  the  growth  of  nerve  fibers  from  cells  of 
the  spinal  ganglion  mesiad  into  the  dorsal  part  of  the  lateral 
plate  of  the  cord.  At  the  same  time  fibers  grow  distad  from 
these  cells  to  form  the  peripheral  part  of  the  nerve  (Fig.  44). 
The  fibers  which  arise  from  the  dorsal  root  ganglion  conduct 
sensory  impulses  toward  the  cord. 

Coincident  with  the  establishment  of  the  dorsal  root,  the 
ventral  root  is  formed  by  fibers  which  grow  out  from  cells 
located  in  the  ventral  part  of  the  lateral  plate  of  the  cord 
(Fig.  44)'.  The  fibers  which  thus  arise  from  cells  in  the  cord 
and  pass  out  through  the  ventral  root,  conduct  motor  impulses 
from  the  brain  and  cord  to  the  muscles  with  which  they  are 
associated  peripherally. 

The  sympathetic  ganglia  arise  from  cells  of  the  neural  crest 
which  migrate  ventrally  and  form  cellular  masses  lying  on 
either  side  of  the  mid-line  at  the  level  of  the  dorsal  aorta. 
By  the  end  of  the  fourth  day  these  cells  constitute  a  pair  of 
cords  in  which  enlargements  can  be  made  out  opposite  the  spinal 
ganglia.  These  enlargements  are  the  primary  sympathetic 
gangha.  Each  sympathetic  ganghon  is  connected  with  the 
corresponding  spinal  nerve  by  a  cellular  cord  which  is  the 
primordium  of  the  ramus  communicans.  The  sympathetic 
ganglia  later  receive  both  sensory  and  motor  fibers  from  the 
spinal  nerve  roots  by  way  of  the  rami  communicantes,  and  from 
nerve  cells  in  the  sympathetic  ganglia,  fibers  extend  to  the 
viscera. 

III.  The  Sense  Organs 

The  Eye. — The  primary  optic  vesicles  arise  in  chicks  of  about 
30  hours  as  dilations  in  the  lateral  wall  of  the  prosencephalon 
(Figs.  19  and  23).  At  first  the  optic  vesicles  open  broadly 
into  the  brain,  but  later  constrictions  develop  which  narrow 
their  attachment  to  the  form  of  a  stalk  (Fig.  22).  In  chicks 
of  55  hours  the  primary  optic  vesicles  are  invaginated  to  form 
the  double-walled  secondary  optic  vesicles  or  optic  cups.  The 
invagination  takes  place  in  such  a  way  that  the  ventral  wall 


STRUCTURE   OF   FOUR-DAY   CHICKS 


121 


of  the  cup  is  incomplete,  the  gap  in  it  being  known  as  the  choroid 
fissure  (Figs.  35  and  36,  B). 

The  lens  arises  as  a  thickening  of  the  superficial  ectoderm 
which  becomes  depressed  to  form  a  vesicular  invagination  ex- 
tending into  the  optic  cup  (Fig.  36,  B). 


ectoderm 


diocoele 
mesenchyme 


concentration  of 

mesenchyme 
pigment  layer 
sensory  layer 

lens 

area  enlarged  in  B 

corneal  region 

optic  stalk 


'•^ 


M 


P-gr 


^m 


'  'ill 


pigment 
layer  of  retina 


sensory 
layer  of  retina 


developing 
lens  fibers 


Pig.  45. — Drawings  to  show  structure  of  the  eye  of  a  four-day  chick. 
A,  diagram  to  show  topography  of  eye  region;  B,  drawing  to  show  cellular 
organization  of  the  pigment  and  sensory  layers  of  the  retina.     Abbreviations: 
mes.,  mesenchymal  cell;  p.gr.,  pigment  granule;  C,  drawing  to  show  cellular 
organization  of  the  lens. 

In  chicks  of  four  days  the  choroid  fissure  has  become  nar- 
rowed by  the  growth  of  the  walls  of  the  optic  cup  on  either  side 
of  it  (Figs.  40  and  42,  B).     The  orifice  of  the  optic  cup  becomes 


122  EARLY   EMBRYOLOGY    OF    THE    CHICK 

narrowed  by  convergence  of  its  margins  toward  the  lens  (Fig. 
45,  A).  Meanwhile  the  lens  has  become  freed  from  the  super- 
ficial ectoderm  and  forms  a  completely  closed  vesicle.  Sections 
of  the  lens  at  this  stage  show  that  the  cells  constituting  that 
part  of  its  wall  which  lies  toward  the  center  of  the  optic  cup 
are  becoming  elongated  to  form  the  lens  fibers  (Fig.  45,  C). 

At  this  stage  we  can  identify  the  beginning  of  most  of  the 
structures  of  the  adult  eye.  The  thickened  internal  layer  of 
the  optic  cup  will  give  rise  to  the  sensory  layer  of  the  retina 
(Fig.  45,  B).  Fibers  arise  from  nerve  cells  in  the  retina  and 
grow  along  the  groove  in  the  ventral  surface  of  the  optic  stalk 
toward  the  brain  to  form  the  optic  nerve.  The  external  layer 
of  the  optic  cup  gives  rise  to  the  pigment  layer  of  the  retina. 
Mesenchyme  cells  can  be  seen  aggregating  about  the  outside  of 
the  optic  cup.  From  these  the  sclera  and  choroid  coat  are 
derived.  Some  of  the  mesenchyme  makes  its  way  into  the 
optic  cup  through  the  choroid  fissure  and  gives  rise  to  the  cellu- 
lar elements  of  the  vitreous  body.  The  comple:?^  ciHary  appar- 
atus of  the  adult  eye  is  derived  from  the  margins  of  the  optic 
cup  adjacent  to  the  lens.  The  corneal  and  conjunctival  epi- 
thelium arise  from  the  superficial  ectoderm  overlying  the  eye. 
Mesenchyme  cells  which  make  their  way  between  the  lens  and 
the  corneal  epithelium  give  rise  to  the  substantia  propria  of  the 
cornea. 

The  Ear.- — Of  the  structures  taking  part  in  the  formation  of 
the  ear,  the  first  to  appear  is  the  auditory  placode.  The  audi- 
tory placode  is  recognizable  in  36-hour  chicks  as  a  thickened 
plate  of  ectoderm.  Almost  as  soon  as  it  appears  the  placode 
sinks  below  the  level  of  the  surrounding  ectoderm  to  form  the 
floor  of  the  auditory  pit  (Fig.  22).  By  constriction  of  its  open- 
ing to  the  surface  the  epithelium  of  the  auditory  pit  becomes 
separated  from  the  ectoderm  of  the  head  and  comes  to  lie  close 
to  the  lateral  wall  of  the  myelencephalon  (Fig.  36,  ^).  A  tubu- 
lar stalk,  the  endolymphatic  duct,  remains  for  a  time  adherent 
to  the  superficial  ectoderm,  marking  the  location  of  the  original 
invagination  (Fig.  40). 

The  degree  of  development  reached  by  the  ear  primordium 
in  four-day  chicks  gives  little  indication  of  the  nature  of  the 
later  processes  by  which  the  ear  is  formed.  The  auditory 
vesicle  by  a  very  complex  series  of  changes  will  give  rise  to  the 


STRUCTURE    OF   FOUR-DAY   CHICKS  1 23 

entire  epithelial  portion  of  the  internal  ear  mechanism.  Nerve 
fibers  arising  from  the  acoustic  ganglion  grow  into  the  brain 
proximally  and  to  the  internal  ear  distally  establishing  nerve 
connections  between  them.  There  is  at  this  stage  no  indication 
of  the  differentiation  of  the  external  auditory  meatus.  The 
dorsal  and  inner  portion  of  the  hyomandibular  cleft  which 
gives  rise  to  the  eustachian  tube  and  to  the  middle  ear  chamber 
has  not  yet  become  associated  with  the  auditory  vesicle. 

The  Olfactory  Organs. — The  olfactory  organs  are  represented 
in  three-day  and  four-day  chicks  by  a  pair  of  depressions  in  the 
ectoderm  of  the  head.  These  so-called  olfactory  pits  are  located 
ventral  to  the  telencephalic  vesicles  and  just  anterior  to  the 
mouth  (Figs.  40  and  41).  By  growth  of  the  processes  which 
surround  them,  the  olfactory  pits  become  greatly  deepened. 
The  epitheHum  lining  the  pits  eventually  comes  to  lie  at  the 
extreme  upper  part  of  the  nasal  chambers  and  constitutes  the 
olfactory  epithelium.  Nerve  fibers  grow  from  these  cells  to 
the  telencephalic  lobes  of  the  brain  to  form  the  olfactory  nerves. 

IV.  The  Digestive  and  Respiratory  Systems 

Summary  of  Development  Prior  to  the  Third  Day. — The 

primary  entoderm  which  gives  rise  to  the  epithelial  Hning  of  the 
digestive  and  respiratory  systems  and  their  associated  glands 
becomes  estabhshed  as  a  separate  layer  before  the  egg  is  laid. 
In  its  early  relationships  the  entoderm  is  a  sheet-like  layer  of 
cells  lying  between  the  ectoderm  and  the  yolk  and  attached 
peripherally  to  the  yolk  (Fig.  7).  The  primitive  gut  is  the 
cavity  bounded  dorsally  by  the  entoderm  and  ventrally  by  the 
yolk  (Fig,  31,  A). 

Only  the  part  of  the  entoderm  which  lies  within  the  em- 
bryonal area  is  involv-ed  in  the  formation  of  the  enteric  tract. 
The  peripheral  portion  of  the  entoderm  goes  into  the  formation 
of  the  yolk-sac.  There  is  at  first  ho  definite  line  of  demarcation 
between  the  entoderm  destined  to  be  incorporated  into  the 
body  of  the  embryo  and  that  which  remains  extra-embryonic 
in  its  associations.  The  foldings  which  appear  later  separating 
the  body  of  the  embryo  from  the  yolk,  establish  for  the  first 
time  the  boundaries  between  intra-embryonic  and  extra-em- 
bryonic entoderm  (Figs.  30  and  32). 


124  EARLY  EMBRYOLOGY   OF   THE   CHICK 

The  first  part  of  the  gut  to  acquire  a  complete  entodermic 
lining  is  the  fore-gut.  Its  floor  is  formed  by  the  caudally 
progressing  concrescence  of  the  entoderm  which  takes  place  as 
the  subcephalic  and  lateral  body  folds  undercut  the  cephalic 
part  of  the  embryo  (Figs.  i6  and  31,  5).  At  a  considerably 
later  stage  the  hind-gut  is  formed  by  the  progress  of  the  sub- 
caudad  fold  (Figs.  35  and  31,  C).  Between  the  fore-gut  and  the 
hind-gut,  the  mid-gut  remains  open  to  the  yolk  ventrally.  As 
the  embryo  is  more  completely  separated  from  the  yolk  the 
fore-gut  and  hind-gut  increase  in  extent  at  the  expense  of  the 
mid-gut.  By  the  fourth  day  of  incubation  the  mid-gut  is  re- 
duced to  the  region  where  the  yolk  stalk  opens  into  the  enteric 
tract  (Figs.  31,  -D  and  43). 

The  Establishment  of  the  Oral  Opening. — When  first  estab- 
lished the  gut  ends  as  a  blind  pocket  both  cephalically  and 
caudally.  The  mouth  opening  does  not  appear  until  the  third 
day,  the  cloacal  opening  is  not  established  until  much  later  in 
incubation.  In  embryos  of  55  hours  the  processes  leading  to- 
ward the  establishment  of  the  oral  opening  are  clearly  indicated. 
A  mid-ventral  evagination  of  the  pharynx  is  estabhshed  im- 
mediately cephalic  to  the  mandibular  arch  (Fig.  35).  Opposite 
this  out-pocketing  of  the  pharynx,  and  growing  in  to  meet  it,  the 
stomodeal  depression  is  formed.  The  thin  membrane  formed 
by  the  meeting  of  the  pharyngeal  entoderm  with  the  stomodeal 
ectoderm  is  known  as  the  oral  plate.  The  communication  of  the 
fore-gut  with  the  outside  is  finally  established  by  the  breaking 
through  of  the  oral  plate. 

The  formation  of  the  mouth  opening  in  the  manner  described 
does  not  take  place  at  the  extreme  anterior  end  of  the  fore-gut. 
A  small  gut  pocket  extends  cephalic  to  the  mouth.  ^  This  so- 
called  pre-oral  gut  rapidly  becomes  less  conspicuous  after  the 
breaking  through  of  the  oral  plate.  The  small  depression 
which  in  older  embryos  marks  its  location  is  known  as  Sees- 
selFs  pocket  (Fig.  43).  Even  this  small  depression  eventually 
disappears  altogether.  Its  importance  lies  wholly  in  the  fact 
that  it  indicates  for  some  time  the  place  at  which  ectoderm 
and  entoderm  originally  became  continuous  in  the  formation 
of  the  oral  opening. 

The  Pharyngeal  Derivatives. — Several  structures  arise  in  the 
pharyngeal  region  which  do  not  become  parts  of  the  digestive 


STRUCTURE    OF   FOUR-DAY   CHICKS  1 25 

system.  Nevertheless  the  origin  of  their  epithelial  portions 
from  fore-gut  entoderm  and  their  early  association  with  this 
part  of  the  gut  tract  makes  it  convenient  to  take  them  up  in 
connection  with  the  digestive  system. 

The  thyroid  gland  arises  as  a  median  diverticulum  from  the 
floor  of  the  pharynx  which  makes  its  appearance  at  the  level  of 
the  second  pair  of  pharyngeal  pouches.  Toward  the  end  of 
the  fourth  day  the  thyroid  evagination  has  become  saccular  and 
retains  its  connection  with  the  pharynx  only  by  a  narrow  open- 
ing at  the  root  of  the  tongue  known  as  the  thyro-glossal  duct 
(Fig.  43).  In  mammaha  the  thyroid  is  contributed  to  by  pri- 
mordia  which  arise  laterally  from  the  fourth  pharyngeal  pouches 
as  well  as  by  a  median  evagination  from  the  floor  of  the 
pharynx.  It  is  possible  that  evaginations  which  in  the  chick 
arise  from  the  fourth  pharyngeal  pouches  are  homologous  with 
the  lateral  thyroid  primordia  of  mammals.  In  the  chick,  how- 
ever, these  evaginations  do  not  form  typical  thyroid  tissue. 

The  thymus  of  the  chick  does  not  appear  until  after  the  fourth 
day  of  incubation.  It  takes  its  origin  primarily  from  divertic- 
ula arising  from  the  posterior  faces  of  the  third  and  fourth 
pharyngeal  pouches.  The  original  epithelial  character  of  the 
thymus  is  soon  largely  lost  in  an  extensive  ingrowth  of  mesen- 
chyme and  the  organ  becomes  chiefly  lymphoid  in  its  histolog- 
ical characteristics. 

The  Trachea. — The  first  indication  of  the  formation  of  the 
respiratory  system-  is  an  outgrowth  from  the  pharynx.  In 
chicks  of  3  days  a  mid- ventral  groove  is  formed  in  the  pharynx, 
beginning  just  posterior  to  the  level  of  the  fourth  pharyngeal 
pouches  and  extending  caudad.  This  groove  deepens  rapidly 
and  by  closure  of  its  dorsal  margins  becomes  separated  from  the 
pharynx  except  at  its  cephaUc  end.  The  tube  thus  formed  is 
the  trachea,  and  the  opening  which  persists  between  the  cephal- 
ic end  of  the  trachea  and  the  pharynx  is  the  glottis  (Fig.  43). 
The  original  entodermal  evagination  gives  rise  only  to  the 
epithelial  lining  of  the  trachea,  the  supporting  structures  of  the 
tracheal  walls  being  derived  from  the  surrounding  mesenchyme. 

The  Lung-buds. — The  tracheal  evagination  grows  caudad 
and  bifurcates  to  form  a  pair  of  lung-buds.  As  the  lung-buds 
develop  they  grow  into  the  loose  mesenchyme  on  either  side  of 
the  mid-line.     The  adjacent  splanchnic  mesoderm  is  pushed 


126  EARLY   EMBRYOLOGY    OF    THE    CHICK 

ahead  of  them  in  their  caudo-lateral  growth  and  comes  to 
constitute  the  outer  investment  of  the  lung-buds.  The  ento- 
dermal  buds  give  rise  only  to  the  epithehal  Hning  of  the  bronchi, 
and  the  air  passages  and  air  chambers  of  the  lungs.  The 
connective  tissue  stroma  of  the  lungs  is  derived  from  mesen- 
chyme surrounding  the  lung-buds,  and  their  pleural  covering 
from  the  investment  of  splanchnic  mesoderm. 

The  Oesophagus  and  Stomach. — Immediately  caudal  to  the 
glottis  is  a  narrowed  region  of  the  fore-gut  which  becomes  the 
oesophagus,  and  farther  caudally  a  slightly  dilated  region  which 
becomes  the  stomach  (Fig.  43).  The  concentration  of  mesen- 
chyme cells  about  the  entoderm  of  the  oesophageal  and  stomach 
regions  foreshadows  the  formation  of  their  muscular  and  con- 
nective tissue  coats  (Fig.  46,  C). 

The  Liver. — In  all  vertebrates  the  Hver  arises  as  a  diverticu- 
lum from  the  ventral  wall  of  the  gut  immediately  caudal  to  the 
stomach  region.  In  chick  embryos  the  liver  diverticulum 
appears  just  as  the  part  of  the  gut  from  which  it  arises  is 
acquiring  a  floor  by  the  concrescence  of  the  margins  of  the 
anterior  intestinal  portal.  As  a  result  the  liver  evagination 
appears  for  a  short  time  on  the  Up  of  the  intestinal  portal,  and 
grows  cephalad  toward  the  fork  where  the  omphalomesenteric 
veins  enter  the  sinus  venosus.  As  closure  of  the  gut  floor  is 
completed,  the  Kver  diverticulum  comes  to  lie  in  its  character- 
istic position  in  the  ventral  wall  of  the  gut.  In  embryos  of  four 
days  the  original  evagination  has  grown  out  in  the  form  of 
branching  cords  of  cells  and  become  quite  extensive  in  mas^ 
(Fig.  43).  In  its  growth  the  liver  pushes  ahead  of  it  the 
splanchnic  mesoderm  which  surrounds  the  gut,  with  the  result 
that  the  hver  from  its  first  appearance  is  invested  by  mesoderm. 
(Fig.46,£). 

The  proximal  portion  of  the  original  evagination  remains  open 
to  the  intestine,  and  serves  as  the  duct  of  the  hver.  This 
primitive  duct  later  undergoes  regional  differentiation  and  gives 
rise  in  the  adult  to  the  common  bile  duct,  to  the  hepatic  and  cys- 
tic ducts,  and  to  the  gall  bladder.  The  cellular  cords  which  bud 
off  from  the  diverticulum  become  the  secretory  units  of  the 
liver  (hepatic  tubules). 

The  same  process  of  concrescence  which  closes  the  floor  of 
the  fore-gut  involves  the  proximal  portion  of  the  omph3.Io- 


STRUCTURE   OF   FOUR-DAY   CHICKS  I27 

mesenteric  veins  which,  when  they  first  appear,  lie  in  the  lateral 
folds  of  the  anterior  intestinal  portal  (Fig.  35).  As  the  intes- 
tinal portal  moves  caudad  in  the  lengthening  of  the  fore-gut, 
the  proximal  portions  of  the  omphalomesenteric  veins  are 
brought  together  in  the  mid-line  and  become  fused.  The  fusion 
extends  caudad  nearly  to  the  level  of  the  yolk  stalk  (Fig.  47). 
Beyond  this  point  they  retain  their  original  paired  condition. 
In  its  growth  the  liver  surrounds  the  fused  portion  of  the  om- 
phalomesenteric veins  (Figs.  43  and  46,  D,  and  E).  This  early 
association  of  the  omphalomesenteric  veins  with  the  liver 
fore-shadows  the  way  in  which  the  proximal  part  of  the  afferent 
vitelline  circulation  is  to  be  involved  in  the  establishment  of  the 
hepatic-portal  circulation  of  the  adult. 

The  Pancreas. — The  pancreas  is  derived  from  evaginations 
appearing  in  the  walls  of  the  intestine  at  the  same  level  as  the 
liver  diverticulum.  There  are  three  pancreatic  buds,  a  median 
dorsal,  and  a  pair  of  ventro-lateral  buds.  The  dorsal  evagina- 
tion  appears  at  about  72  hours,  the  ventro-lateral  evaginations 
toward  the  end  of  the  fourth  day.  The  dorsal  pancreatic  bud 
arises  directly  opposite  the  liver  diverticulum  and  grows  into 
the  dorsal  mesentery  (Fig.  43).  The  ventro-lateral  buds  arise 
where  the  duct  of  the  liver  connects  with  the  intestine  so  that 
the  ducts  of  the  liver  and  the  ventral  pancreatic  ducts  open 
into  the  intestine  by  a  common  duct  (ductus  choledochus). 
Later  in  development  the  masses  of  cellular  cords  derived 
from  the  three  pancreatic  primordia  grow  together  and 
become  fused  into  a  single  glandular  mass,  but  usually  two 
and  in  rare  cases  all  three  of  the  original  ducts  persist  in  the 
adult. 

The  Mid-gut  Region. — In  chicks  of  four  days  the  enteric 
tract  shows  no  local  differentiation  from  the  level  of  the  liver 
to  the  cloaca  except  where  the  yolk-sac  is  attached.  All  of  the 
gut  tract  between  the  stomach  and  the  yolk-stalk,  and  the 
anterior  third  of  the  gut  lying  caudal  to  the  yolk-stalk  is  des- 
tined to  become  the  small  intestine.  The  posterior  two-thirds 
of  the  hind-gut  becomes  large  intestine  and  cloaca. 

The  Cloaca. — The  beginning  of  the  formation  of  the  cloaca 
is  indicated  in  chicks  of  four  days  incubation,  by  a  dilation  of 
the  posterior  portion  of  the  hind-gut  (Fig.  43).  Although  ex- 
tensive differentiations  in  the  cloacal  region  do  not  appear 


128 


ganglion  VII-VIII 
auditoty  vesicle 


EARLY  EMBRYOLOGY   OF  THE   CHICK 

ganglion  V 


myelocoele 


branch  of 

int.  carotid  a. 


anterior  cardinal  vem 


branch  of 
ant.  cardinal  v. 
metacoele 


neuromere 


aortic  arch  11 

aortic  arch 

"^\          ^V 

aortic  arch  IV 

^^-^.^^  ^\^J— ^ 

dorsal               ^^ 
ganglion  ^.,.^^^—-5 

neural            /S^Sm 

notochord  ^ 

^F 

dorsal  aorta/       /           /  ^"^m^ 
ant.  cardinal  vV           y^        J      \ 

visceral 

cleft  III/             /           \ 

B 

visceral  arch  WV                    \ 

visceral  cleft 

pericardial 

region  of  coelom.^^ 

trachea^                    \     ^^^ 

oesophagus 

j^^^^N^^j;^— ^kj 

neural           i^^ 
tube— ^S 

^^^^r  1 

pharynx 


int.  carotid  a. 

ant.  cardinal  v. 
mesococle 


■'?;^ 


dorul  aorta' 


atnum 
bulbo-conus  arteriosus 


pharyngeal  pouch  I 


mandibular  arch 
'hyomandibular  cleft 
hyoid  arch 


diocoele 


ventral  body  wall ' 


optic  stalk 

sensory  layer  of  retina 

pigment  layer  of  retina 


olfactory  pit 


bulbo-conus  arteriosus 
sinus  venosus 
right  duct  of  Cuvier 
posterior 
cardinal  v, 


lung  bud 

pleural  region 

Dof  coelom       left    duct 
of  Cuvier 


diocoele 


pericardial  region  of  coelom 

Fig.  46 


STRUCTURE    OF  FOUR-DAY  CHICKS 


129 


ductus  choledochus 
mesonephric  duct 
dorsal  mesentery 

dorsal  ganglion 

neural  tube 


omphaloniesenteric  vein 
ventricle 


lateral  telencephalic 
vesicle 


ectoderm  of  hea4 


G 


dorsal 
ganglion 
post,  cardinal  v. 

dorsal  aorta 
mesonephric  duct 

allantoic  vein 


vitelline 
vessels 


omphalomesenteric  veins 


entoderm 


sub^  intestinal 

vein 
allantoic  vein 
allantoic  stalk 


allantoic  art. 
coelom 
post,  appendage 


Fig.  46. — Diagrams  of  transverse  sections  of  a  four-day  chick.     The  location  of 
the  sections  is  indicated  on  a  small  outline  sketch  of  the  entire  embryo. 


130  EARLY   EMBRYOLOGY   OF   THE   CHICK 

until  later  in  development,  certain  of  its  fundamental  relation- 
ships are  established  at  this  stage. 

The  cloaca  of  an  adult  bird  is  the  common  chamber  into 
which  the  intestinal  contents,  the  urine,  and  the  products  of 
the  reproductive  organs  are  received  for  discharge.  The  first 
appearance  of  the  cloaca  in  the  embryo  as  a  dilated  terminal 
portion  of  the  gut  establishes  at  the  outset  the  relations  of 
cloaca  and  intestine  familiar  in  the  adult. 

Although  the  urinary  system  is  not  at  this  stage  developed 
to  conditions  which  resemble  those  in  the  adult  the. parts  of  it 
which  have  been  estabhshed  are  already  definitely  associated 
with  the  cloaca.  The  proximal  portion  of  the  allantoic  stalk 
which  is  the  homologue  of  the  urinary  bladder  of  mammals 
opens  directly  into  the  cloaca  (Fig.  43).  When  the  urinary 
system  of  the  embryo  is  considered,  we  shall  see  that  the  ducts 
which  drain  the  developing  excretory  organs  also  open  into 
the  cloacal  region  on  either  side  of  the  allantoic  stalk. 

There  is  at  this  stage  but  little  indication  of  the  for- 
mation of  the  gonads.  The  relation  of  the  sexual  ducts 
to  the  cloaca  can  be  made  out  only  by  the  study  of  older 
embryos. 

The  Proctodaeum  and  the  Cloacal  Membrane. — Indications 
of  the  formation  of  the  cloacal  opening  to  the  outside  appear 
during  the  fourth  day  of  incubation.  Its  establishment  is 
accomplished  in  much  the  same  manner  as  the  establishment 
of  the  oral  opening.  A  ventral  out-pocketing  of  the  hind-gut 
arises  just  caudal  to  the  point  at  which  the  allantoic  stalk 
opens  into  the  cloaca  (Fig.  43) .  At  the  same  time  a  depression 
appears  in  the  overlying  ectoderm.  The  external  depression 
which  grows  in  toward  the  gut  pocket  is  known  as  the  procto- 
daeum.  The  double  epithelial  layer  formed  by  the  meeting  of 
gut  entoderm  with  proctodeal  ectoderm  is  the  cloacal  mem- 
brane. The  formation  of  the  proctodaeum  and  the  cloacal 
membrane  cleaily  indicate  the  location  of  the  future  cloacal 
opening  although  an  open  communication  is  not  established 
by  the  rupture  of  the  cloacal  membrane  until  considerably 
later.  The  cloacal  opening  does  not  form  at  the  extreme  pos- 
terior end  of  the  hind-gut  and  there  is,  therefore,  a  post-anal 
pocket  of  the  hind-gut  suggestive  of  the  pre-oral  pocket  of  the 
fore-gut. 


STRUCTURE   OF  FOUR-DAY   CHICKS  I3I 

V.  The  Circul-\tory  System 

The  Functional  Significance  of  the  Embryonic  Circulation. 
The  arrangement  of  the  embnonic  circulation  is  dimciilt  to 
understand  only  when  its  functional  significance  is  overlooked. 
In  the  embtyo  as  in  the  adult  the  main  circulatory  channels 
lead  to  and  from  the  centers  of  metabohc  acti\^ty.  The  circu- 
lating blood  carries  material  from  the  organs  of  digestion  and 
absorption  to  remote  parts  of  the  body;  ox\'gen  to  all  parts 
of  the  body  from  the  organs  which  are  specially  constructed 
to  take  up  oxygen  from  the  surroimding  medium;  and  waste 
materials  from  the  places  of  their  h*beration,  to  the  organs 
through  which  they  are  eliminated.  The  differences  between 
the  course  of  the  circulation  in  the  embr\'o  and  in  the  adult  are 
due  to  the  fact  that  their  centers  of  metaboUc  activity  are 
differently  located. 

The  organs  which  in  the  adult  cany  out  such  functions  as 
digestion  and  absorption,  respiration,  and  excretion  are  ex- 
tremely complex  and  highly  differentiated  structures.  They 
are  for  this  reason  slow  to  attain  their  definitive  condition  and 
do  not  become  functional  until  toward  the  close  of  embryonic 
life.  Moreover  the  conditions  by  which  the  developing  adult 
organs  are  surrounded  during  embryonic  life  are  in  some  in- 
stances an  absolute  bar  to  their  becoming  functional  were  they 
sufficiently  developed  so  to  do.  Suppose  the  lungs,  for  example, 
were  fuUy  formed  at  an  early  stage  of  development.  The  fact 
that  the  chick  embr\^o  is  living  submerged  in  the  anmiotic  fluid 
would  render  them  as  incapable  of  fxmctioning  as  the  lungs  of  a 
man  under  water.  Were  the  embrj'o  dependent  on  the  es- 
tablishment of  the  organs  which  carry  on  metabolism  in  the 
adult,  development  would  be  at  an  impasse.  To  develop,  the 
embr>'o  must  have  not  only  the  raw  food  material  suppHed  it 
by  the  mother  in  the  form  of  yolk,  it  must  have  a  means  of 
digesting  the  yolk,  absorbing  it,  and  canying  it  to  the  places 
where  it  can  be  utilized.  The  utilization  of  food  material  to 
produce  the  energy-  expressed  in  growth  processes  depends  on 
presence  of  ox\-gen.  For  growth  there  must  be  a  means  of 
securing  oxygen  and  canying  it,  as  weU  as  food,  to  all  parts  of 
the  body.  Xor  can  continued  growth  go  on  unless  the  waste 
products  Hberated  by  the  growing  tissues  are  elinunated.     At 


132  EARLY  EMBRYOLOGY   OF   THE   CHICK 

the  outset  of  its  development  the  embryo  must,  therefore, 
establish  organs  for  the  digestion  and  absorption  of  food,  the 
securing  of  oxygen,  and  the  elimination  of  waste  products. 
These  organs  serve  the  embryo  but  temporarily  and  are  dif- 
ferent in  structure  and  in  location  from  the  organs  which  carry 
out  the  corresponding  functions  in  the  adult,  their  nature  and 
location  depending  on  the  exigencies  of  the  embryo's  living 
conditions. 

The  main  channels  of  the  circulation  in  young  embryos  lead 
to  and  from  their  temporary  organs  of  digestion  and  absorption, 
respiration,  and  excretion.  The  arrangement  of  the  main 
vessels  characteristic  of  the  adult  appears  only  as  the  organs 
characteristic  of  the  adult  develop.  The  changes  by  which  the 
circulatory  system  acquires  its  adult  arrangement  are  of  neces- 
sity gradual.  Any  changes  which  were  sufficiently  abrupt  to 
interfere  with  the  circulation  would  result  in  disaster  for  the 
embryo.  Even  slight  curtailment  of  the  normal  blood  supply 
to  any  region  would  cause  its  growth  to  cease;  any  marked  local 
decrease  in  the  circulation  would  result  in  local  atrophy  or 
malformation;  complete  interruption  of  any  important  circula- 
tory channel,  even  for  a  short  time,  would  inevitably  mean  the 
death  of  the  embryo.  Consequently  the  arrangement  of 
vessels  characteristic  of  the  embryo  persists  during  the  forma- 
tion of  the  adult  organs,  and  becomes  altered  only  gradually  as 
the  adult  organs  and  the  vessels  associated  with  them  become 
ready  to  function. 

If  the  various  circulatory  channels  of  young  chick  embryos 
are  considered  in  the  light  of  their  functions,  the  differences 
between  the  embryonic  and  the  adult  circulations  should  not 
be  troublesome.  The  circulation  of  young  chick  embryos  in- 
volves three  main  arcs  of  which  the  heart  is  the  common  center 
and  pumping  station.  One  of  these  circulatory  arcs,  the  vitel- 
line, carries  blood  to  the  yolk-sac  where  food  materials  are 
absorbed  and  then  returns  the  food-laden  blood  to  the  heart  for 
distribution  within  the  embryo.  Another  arc  carries  blood  to 
and  from  the  allantois.  The  distal  portion  of  the  allantois  lies 
close  beneath  the  egg  shell  and  the  blood  circulating  in  the 
allantoic  vessels  is  thereby  brought  into  a  location  where  inter- 
change of  gases  can  be  carried  on  with  the  air  which  penetrates 
the  shell  (Fig.  30,  C  and  D).     It  is  in  the  allantoic  circulation 


STRUCTURE    OF   FOUR-DAY   CHICKS  133 

that  the  blood  gives  off  its  carbon  dioxide  and  acquires  a  fresh 
supply  of  oxygen.  The  allantoic  circulation  is  also  the  em- 
bryo's means  of  eliminating  nitrogenous  waste  material  from 
the  blood.  The  remaining  circulatory  arc  is  confined  to  the 
body  of  the  embryo.  The  intra-embryonic  circulation  has 
many  distributing  and  collecting  vessels  but  all  of  them  are 
alike  in  function  in  that  they  bring  food  material  to,  and 
carry  waste  material  from,  the  various  parts  of  the  developing 
body.  Nowhere  in  their  course  are  the  vessels  of  the  intra- 
embryonic  circulation  involved  in  adding  food  material  or 
oxygen  to  that  already  contained  in  the  blood  they  convey,  and 
nowhere  do  they  free  the  blood  from  waste  materials  until  well 
along  in  development,  when  the  nephroi  become  functional. 

In  the  heart  the  blood  from  the  three  circulatory  arcs  is 
mingled.  As  it  leaves  the  heart  the  mixed  blood  is  not  as  rich  in 
food  material  as  the  blood  coming  in  through  the  omphalo- 
mesenteric veins,  nor  as  free  from  waste  materials  and  as  rich 
in  oxygen  as  the  blood  returned  over  the  allantoic  veins.  Its 
condition  of  serviceability  to  the  embryo  is,  however,  constantly 
maintained  at  a  good  average  by  the  incoming  viteUine  and 
allantoic  blood. 

There  is  a  tendency  among  students  who  have  done  but 
little  work  on  the  circulation  to  regard  any  vessel  which  carries 
oxygenated  blood  as  an  artery,"  ailti  any  vessel  which  carries 
blood  poor  in  oxygen  and  high  in  carbon  dioxide  content  as  a 
vein.  This  is  not  entirely  correct  even  for  the  circulation  of 
adult  mammals  on  which  the  conception  is  based.  In  com- 
parative anatomy  and  especially  in  embryology  it  is  far  from 
being  the  case.  It  is  necessary,  therefore,  in  dealing  with  the 
circulation  of  the  embryo  to  eradicate  this  not  uncommon 
misconception. 

The  differentiation  between  arteries  and  veins  which  holds 
good  for  all  forms,  both  embryonic  and  adult,  is  based  on  the 
structure  of  their  walls,  and  on  the  direction  of  their  blood  flow 
with  reference  to  the  heart.  An  artery  is  a  vessel  carrying 
blood  away  from  the  heart  under  a  relatively  high  fluctuating 
pressure  due  to  the  pumping  of  the  heart.  Correlated  with  the 
pressure  conditions  in  it,  its  walls  are  heavily  reinforced  by 
elastic  and  muscle  tissue.  A  vein  is  a  vessel  carrying  blood 
toward     the      heart     under     relatively     low     and      constan 


134 


EARLY   EMBRYOLOGY   OF   THE   CHICK 


pressure  from  the  blood  welling  into  it  from  capillaries.  Corre- 
lated with  the  pressure  conditions  characteristic  for  it,  the  walls 
of  a  vein  have  much  less  elastic  and  muscle  tissue  than  artery 
walls,  and  more  non-elastic  fibers  reinforcing  them. 

The  Vitelline  Circulation. — The  earHest  indication  of  blood 
and  blood  vessel  formation  is  at  the  chick's  source  of  food  supply. 
Blood  islands  appear  in  the  extra-embryonic  splanchnopleure 


pharyngeal  pouches     I -IV 

ant.  cardinal  v 
aortic  arch  IV 


aortic  arch  I 
^disappearing  j 


int  carotid  a. 


ext.  carotid  a. 


dorsal 
aorta  . 


mesoncphros 


^..Au*^ 


post,  cardinal  v 
hind-KUt 


ext.   iliac     artery 
cloaca     — 


allantoic  artery         ^ 
proctodaeum         OUMV\iA 
post -anal  gut 


Pig.  47. — Schematic  diagram  to  show  the  location  of  the  more  prominent 
internal  organs  of  the  four-day  chick.  Except  for  the  omphalomesenteric 
arteries  and  veins  paired  structures  are  represented  only  on  the  side  toward  the 
observer. 

of  the  yolk-sac  toward  the  end  of  the  first  day  of  incuba- 
tion, and  rapidly  become  differentiated  to  form  vascular  endo- 
thehum  enclosing  central  clusters  of  primitive  blood  corpuscles 
(Fig.  25).  By  extension  and  anastomosing  of  neighboring 
islands  a  plexus  of  blood  channels  is  formed  in  the  yolk-sac. 
Further  extension  of  the  vitelUne  plexus  brings  it  into  communi- 
cation with  the  omphalomesenteric  veins  which  have  been  de- 
veloped in  the  embryo  as  caudal  extensions  of  the  heart  (Fig.  21). 


STRUCTURE   OF   FOUR-DAY   CHICKS 


.135 


Toward  the  end  of  the  second  day  of  development  the  om- 
phalomesenteric arteries  establish  communication  between 
the  dorsal  aortae  and  the  vitelHne  plexus.  (See  Chap.  X  and 
Figs.  29  and  35.)  There  is  now  a  system  of  open  channels  lead- 
ing from  the  embryo  to  the  yolk-sac,  and  back  again  to  the  embryo. 
With  the  completion  of  these  channels  the  heart  begins  to 
pulsate,  circulation  of  the  blood  is  thereby  estabhshed,  and  the 


Pig.  48. — Diagram  to  show  course  of  vitelline  circulation  in  chick  of  about 
four  days.  (After  Lillie.)  For  the  intra-embryonic  vessels  see  Fig.  47.  Abbre- 
viations; A,  dorsal  aorta;  A.V.V.,  anterior  vitelline  vein;  L.V.V.,  lateral  vitelline 
vein;  M.V.,  marginal  vein  (sinus  terminalis);  P.V.V.,  posterior  vitelline  vein; 
V.A.,  vitelline  artery.     The  direction  of  blood  flow  is  indicated  by  arrows. 


blood  cells  formed  in  the  yolk-sac  are  for  the  first  time  carried 
into  the  body  of  the  embryo. 

The  course  of  the  vitelline  circulation  in  chicks  of  four  days 
is  shown  diagrammatically  in  Figures  47  and  48.     Circulating 


Oi 


136  EARLY  EMBRYOLOGY  OF  THE   CHICK 

in  the  rich  plexus  of  small  vessels  on  the  yolk,  the  blood  finally 
makes  its  way  either  directly  into  one  or  another  of  the  larger 
vitelline  veins,  or  to  the  sinus  terminalis  which  acts  as  a  collecting 
channel,  and  then  over  the  sinus  terminalis  to  one  of  the  vitel- 
line veins.  The  vitelline  veins  converge  toward  the  yolk-stalk 
where  they  empty  into  the  omphalomesenteric  veins.  The 
omphalomesenteric  veins  at  first  paired  throughout  their 
entire  length  have  been  brought  together  proximally  by  the 
closure  of  the  ventral  body  wall  and  become  fused  to  form  a 
median  vessel  within  the  body  of  the  embryo.  It  is  through 
this  vessel  that  the  vitelline  blood  eventually  reaches  the 
heart.  In  the  heart  the  blood  of  the  vitelline, intra-embryonic, 
and  allantoic  circulations  is  mingled.  The  mixed  blood  passes 
out  by  the  ventral  aorta  and  the  aortic  arches  into  the  dorsal 
aorta.  Leaving  the  dorsal  aorta  through  the  vitelline  arteries 
the  blood  is  returned  to  the  yolk-sac. 

It  should  not  be  inferred  that  the  blood  stream  ''picks  up" 
deutoplasmic  granules  and  carries  them  to  the  embryo.  The 
acquisition  of  food  material  by  the  blood  depends  on  the  activ- 
j  ities  of  the  entodermal  cells  lining  the  yolk-sac.  These  cells 
secrete  digestive  enzymes  which  break  down  the  deutoplasmic 
granules.  The  liquified  material  is  then  absorbed  by  the  yolk- 
sac  cells  and  transferred  to  the  blood.  The  blood  carries  the 
food  material  in  soluble  form  to  the  embryo  where  it  is  finally 
assimilated. 

The  Allantoic  Circulation. — The  allantoic  arteries  arise  by 
the  prolongation  and  enlargement  of  the  segmental  vessels 
arising  from  the  aorta  at  the  level  of  the  allantoic  stalk.  Their 
size  increases  rapidly  as  the  allantois  increases  in  extent.  From 
them  the  blood  is  distributed  in  a  rich  plexus  of  vessels  which 
ramify  in  the  mesoderm  of  the  allantois  (Fig.  47). 

The  situation  of  the  allantois  directly  beneath  the  porous 
shell  is  such  that  the  blood  can  carry  on  interchange  of  gases 
with  the  outside  air  (Fig.  30,  D).  It  is  in  the  rich  plexus  of 
small  allantoic  vessels  where  the  surface  exposure  is  very  great 
that  the  blood  gives  off  its  carbon  dioxide  and  takes  up  oxygen. 

At  a  later  stage  of  development  the  ducts  of  the  embryonic 
excretory  organs  open  into  the  allantoic  stalk  near  its  cloacal 
end.  As  the  excretory  organs  become  functional  the  allantoic 
vesicle  becomes  the  repository  for  the  nitrogenous  waste  mate- 


STRUCTURE  OF  FOUR-DAY  CHICKS  137 

rials  eliminated  through  them.  The  watery  portion  of  the 
waste  materials  is  passed  off  by  evaporation.  The  remaining 
soHds  are  deposited  in  the  allantoic  vesicle.  They  accumulate 
in  the  extra-embryonic  portion  of  the  allantois  and  there  remain 
until  that  portion  of  the  allantois  is  discarded  at  the  close  of 
embryonic  Hfe. 

The  blood  from  the  allantois  is  collected  and  returned  to  the 
heart  over  the  allantoic  veins.  From  the  distal  portion  of  the 
allantois  the  smaller  veins  converge  and  unite  into  two  main 
vessels,  right  and  left,  which  enter  the  body  of  the  embryo  with 
the  allantoic  stalk  (Fig.  46,  H).  After  their  entrance  into  the 
body  the  allantoic  veins  extend  cephalad  in  the  lateral  body 
walls  (Figs.  47  and  46,  H  to  D).  They  enter  the  sinus  venosus 
on  either  side  of  the  entrance  of  the  omphalomesenteric  vein. 

The  Intra-embryonic  Circulation. — The  earUest  vessels  of 
the  intra-embryonic  circulation  to  appear  are  the  large  vessels 
communicating  with  the  heart.  In  chicks  of  33  hours  the 
ventral  aorta  leads  off  from  the  heart  cephalically  and  bifur- 
cates ventral  to  the  pharynx  giving  rise  to  a  single  pair  of 
aortic  arches.  The  aortic  arches  pass  dorsad  around  the  antero- 
lateral walls  of  the  pharynx  and  are  continued  caudally  along 
the  dorsal  wall  of  the  gut  as  the  paired  dorsal  aortae  (Fig.  23). 

When,  toward  the  end  of  the  second  day  of  incubation,  vis- 
ceral clefts  and  visceral  arches  appear,  the  original  pair  of 
aortic  arches  comes  to  lie  in  the  mandibular  arch.  In  each  of 
the  visceral  arches  posterior  to  the  mandibular,  new  aortic 
arches  are  formed  connecting  the  ventral  aortae  with  the  dorsal 
aortae.  By  55  hours  three  pairs  of  aortic  arches  are  present 
and  a  fourth  is  beginning  to  form  (Fig.  35). 

At  about  this  stage  extensions  of  the  dorsal  aortic  roots  grow 
out  anteriorly.  The  vessels  thus  derived  extend  cephalad  in 
close  association  with  the  brain  as  the  internal  carotid  arteries. 
In  a  later  stage  vessels  arise  from  the  ventral  aortic  roots  and 
grow  cephalad  as  the  external  carotid  arteries  (Fig.  47). 

By  the  end  of  the  fourth  day  of  incubation  two  more  pairs 
of  aortic  arches  have  appeared  posterior  to  the  four  formed  in 
55  to  60-hour  chicks.  From  their  first  appearance  the  fifth 
aortic  arches  are  very  small  and  they  soon  disappear  altogether. 
The  first  and  second  pairs  of  aortic  arches  have  by  this  time 
suffered  a  great  diminution  in  size  which  is  indicative  of  their 


138  EARLY  EMBRYOLOGY   OF   THE   CHICK 

final  disappearance.  In  many  embryos  of  this  age  the  first 
arches,  and  in  a  few  the  second  also,  have  disappeared  alto- 
gether. This  leaves  only  the  third,  fourth,  and  sixth  pairs  of 
aortic  arches.  These  arches  persist  intact  for  some  time,  and 
parts  of  them  remain  permanently,  being  incorporated  in  the 
formation  of  the  aortic  arch  and  the  main  vessels  arising  from 
it,  and  in  the  roots  of  the  pulmonary  arteries. 

In  reptiles,  birds,  and  mammals  the  main  adult  vessels  which 
connect  the  heart  with  the  dorsal  aorta  are  derived  from  the 
fourth  pair  of  aortic  arches  of  the  embryo.  The  paired  condi- 
tion of  these  arches  persists  as  the  adult  condition  in  reptiles, 
but  in  birds  and  mammals  one  of  the  arches  degenerates  before 
the  end  of  embryonic  fife.  In  birds  the  left  arch  degenerates 
leaving  the  right  one  as  the  adult  aortic  arch;  in  mammals  the 
right  arch  degenerates  leaving  the  left  as  the  aortic  arch  of  the 
adult. 

The  dorsal  aortae,  at  first  paired,  later  become  fused  to  form  a 
median  vessel.  The  fusion  begins  at  about  the  level  of  the 
sinus  venosus  and  progresses  cephalad  and  caudad  (Fig.  35). 
Fusion  extends  cephalad  but  a  short  distance,  never  involving 
the  region  of  the  aortic  arches.  Caudally  the  aortae  eventually 
become  fused  throughout  their  entire  length. 

Early  in  development  the  aorta  gives  rise  to  a  segmentally 
arranged  series  of  small  vessels  which  extend  into  the  dorsal 
body  wall.  At  the  level  of  the  anterior  appendage  buds  a  pair 
of  the  segmental  arteries  become  enlarged  and  extend  into  the 
wing  buds  as  the  sub-clavian  arteries.  Coincident  with  the 
development  of  the  allantois,  segmental  vessels  opposite  the 
allantoic  stalk  become  enlarged  and  extend  into  it  as  the  allan- 
toic arteries.  The  external  iliac  arteries  to  the  posterior  ap- 
pendage buds  arise  as  branches  of  the  allantoic  arteries  close  to 
their  origin  from  the  aorta  (Fig.  47) . 

The  three  main  arteries  which  in  the  adult  supply  the  ab- 
dominal viscera  are  represented  in  four-day  chicks  only  by  the 
omphalomesenteric  arteries.  The  omphalomesenteric  arteries 
arise  as  paired  vessels  (Fig.  35),  but  in  the  closure  of  the  ventral 
body  wall  of  the  embryo  they  are  brought  together  and  fused  to 
form  a  single  vessel  which  runs  in  the  mesentery  from  the  aorta 
to  the  yolk-stalk  (Fig.  47).  With  the  atrophy  of  the  yolk-sac 
the  proximal  part  of  the  omphalo-mesenteric  artery  persists  as 


STRUCTURE   OF   POUR-DAY   CHICKS  1 39 

the  superior  mesenteric  of  the  adult.  The  coeliac  and  the 
inferior  mesenteric  arteries  arise  from  the  aorta  independently 
at  a  later  stage. 

The  cardinal  veins  are  the  principal  afferent  systemic  vessels 
of  the  early  embryo.  They  appear  toward  the  end  of  the  second 
day  as  paired  vessels  extending  anteriorly  and  posteriorly  on 
either  side  of  the  mid-line.  At  the  level  of  the  heart  the  anterior 
and  posterior  cardinal  veins  of  the  same  side  of  the  body  become 
confluent  in  the  ducts  of  Cuvier  and  turn  ventrad  to  enter  the 
sinus  venosus  (Figs.  24  and  35) .  Chicks  of  four  days  show  little 
change  in  the  relationships  of  the  cardinal  veins  (Fig.  47). 
Later  in  development  the  proximal  ends  of  the  anterior  cardinals 
become  connected  by  the  formation  of  a  new  transverse  vessel 
and  empty  together  into  the  venous  atrium  of  the  heart.  Their 
distal  portions  remain  in  the  adult  as  the  principal  afferent 
vessels  (jugular  veins)  of  the  cephalic  region. 

The  posterior  cardinals  lie  in  the  angle  between  the  somites 
and  the  lateral  mesoderm  (Fig.  36,  D,  E).  When  the  mesone- 
phroi  develop  from  the  intermediate  mesoderm,  the  cardinal 
veins  lie  just  dorsal  to  them  throughout  their  length  (Figs.  52,  C 
and  46,  E  to  H).  In  young  embryos  the  posterior  cardinals 
are  the  main  afferent  vessels  of  the  posterior  part  of  the  body. 
Later  in  development  they  are  replaced  by  a  new  vesssel,  the 
inferior  vena  cava.  The  changes  by  which  posterior  cardinals 
become  reduced  and  broken  up  to  form  small  vessels  with  new 
associations,  belong  to  stages  of  development  beyond  the  scope 
of  this  book. 

The  Heart. — The  heart  in  adult  vertebrates  is  a  ventral 
unpaired  structure.  Its  origin  in  the  chick  from  paired  primor- 
dia  is  correlated  with  the  way  the  young  embryo  lies  spread  out 
on  the  yolk  surface.  When  the  ventral  body  wall  is  completed 
by  the  folding  together  of  layers  which  formerly  extended  to 
right  and  left  over  the  yolk,  the  paired  primordia  of  the  heart 
are  brought  together  in  the  mid-Hne.  Their  fusion  establishes 
the  heart  as  an  unpaired  structure  lying  in  the  characteristic 
ventral  position  (see  Chap.  IX  and  Figs.  26  and  27). 

After  the  fusion  of  its  paired  primordia  the  heart  is  a  nearly 
straight,  double-walled  tube  (Figs.  49,  A  and  19).  The  primor- 
dial endocardium  of  the  heart  has  the  same  structure  and  arises 
in  the  same  manner  as  the  endothelial  walls  of  the  primitive 


140  EARLY   EMBRYOLOGY   OF   THE   CHICK 

embryonic  blood  vessels  with  which  it  is  directly  continuous. 
The  epi-myocardial  layer  of  the  heart  is  an  outer  investment 
which  surrounds  and  reinforces  the  endocardial  wall.  As 
development  progresses  the  epi-myocardium  becomes  greatly 
thickened  and  is  finally  differentiated  into  two  layers,  a  heavy 
muscular  layer,  the  myocardium,  and  a  thin  non-muscular 
covering  layer,  the  epicardium. 

In  the  apposition  of  the  paired  primordia  of  the  heart  to  each 
other  the  splanchnic  mesodeim  from  either  side  of  the  body 
comes  together  dorsal  and  ventral  to  the  heart.  The  double- 
layered  supporting  membranes  thus  formed  are  known  as  the 
dorsal  mesocardium  and  the  ventral  mesocardium,  respectively 
(Fig.  26).  The  ventral  mesocardium  disappears  shortly  after 
its  formation,  leaving  the  heart  suspended  in  the  body  cavity 
by  the  dorsal  mesocardium  (Fig.  26  E,  D).  Somewhat  later 
the  dorsal  mesocardium  also  disappears  except  at  the  caudal  end 
of  the  heart.  Thus  the  heart  comes  to  lie  in  the  pericardial 
cavity  unattached  except  at  its  two  ends.  The  cephalic  end  of 
the  heart  remains  fixed  with  reference  to  the  body  of  the 
embryo  where  the  ventral  aorta  lies  embedded  ventral  to  the 
floor  of  the  pharynx,  and  the  caudal  end  of  the  heart  is  fixed  by 
the  persistent  portion  of  the  dorsal  mesocardium  and  the 
omphalomesenteric  veins. 

The  straight  tubular  condition  of  the  heart  persists  but  a 
short  time.  The  unattached  ventricular  region  becomes 
dilated  and  is  bent  out  of  the  mid-line  toward  the  embryo's 
right  while  the  fiLxed  bulbo-conus  arteriosus  and  the  sinus 
venosus  are  held  in  their  original  median  position  (Fig.  49, 
A-E).  This  bending  of  the  heart  to  form  a  U-shaped  tube 
begins  to  be  apparent  in  embryos  of  30  hours  and  becomes 
rapidly  more  conspicuous,  until  by  forty  hours  the  ventricular 
region  of  the  heart  lies  well  to  the  right  of  the  embryo's  body 
(Cf.  Figs.  21  and  22). 

The  bending  of  the  heart  to  the  side  involves  a  considerable 
factor  of  ''mechanical  expediency."  The  initiation  of  the 
bending  process  depends  on  the  fact  that  the  heart  is  becoming 
elongated  more  rapidly  than  is  the  chamber  in  which  it  lies 
fixed  by  its  two  ends.  The  fact  that  the  bending  takes  place  to 
the  side  rather  than  dorsally  or  ventrally  may  be  attributed  to 


STRUCTURE    OF   FOUR-DAY   CHICKS  141 

the  impediment  offered  to  its  dorsal  bending  by  the  body  of  the 
embryo,  and  to  its  ventral  bending  by  the  yolk. 

The  lateral  bending  of  the  heart  attains  its  greatest  extent 
at  about  40  hours  of  incubation.  At  this  stage  torsion  of  the 
body  of  the  embryo  changes  the  mechanical  limitations  in  the 
heart  region.  As  the  embryo  comes  to  lie  on  its  left  side  the 
heart  is  no  longer  pressed  against  the  yolk  (Cf.  Figs.  21  and  29). 
As  a  result  the  bend  begins  to  swing  somewhat  ventrad  and  Hes 
less  closely  against  the  body  of  the  embryo  (Figs.  49  and  50, 

At  about  this  stage  of  development  a  new  factor  affects  the 
changes  in  the  shape  of  the  heart.  The  closed  part  of  the 
U-shaped  bend  is  forced  caudad  and  at  the  same  time  becomes 
twisted  on  itself  to  form  a  loop  (Figs.  49,  F-I  and  50,  F-I). 
In  the  formation  of  the  loop  the  atrial  region  is  forced  sHghtly  to 
the  left  {i.e.,  toward  the  yolk)  and  the  conus  is  thrown  across  the 
atrial  region  by  being  bent  to  the  right  {i.e.,  away  from  the  yolk) 
and  then  caudad.  The  ventricular  region  constitutes  the  closed 
end  of  the  loop.  This  twisting  process  reverses  the  original 
cephalo-caudal  relations  of  the  atrial  and  ventricular  regions. 
The  atrial  region  which  was  at  first  caudal  to  the  ventricle  now 
lies  cephalic  to  it  as  in  the  adult  heart. 

The  atrial  region  and  the  ventricular  region  which  formerly 
were  continuous  without  any  line  of  demarcation,  are  by  this  time 
beginning  to  be  marked  off  from  each  other  by  a  constriction 
(Fig.  49,  /,  a.v.).  As  both  the  atrium  and  the  ventricle  be- 
come enlarged,  this  constriction  is  accentuated  (Fig.  49, L,  a.  v.). 
The  constricted  region  is  now  termed  the  atrio-ventricular 
canal. 

During  the  fourth  day  the  bulbo-conus  arteriosus  becomes 
closely  applied  to  the  ventral  surface  of  the  atrium.  As  the 
atrium  grows  it  tends  to  expand  on  either  side  of  the  depression 
made  in  it  by  the  pressure  of  the  bulbo-conus  (Figs.  49,  J-L 
and  50  J-L).  These  lateral  expansions  of  the  atrium  are  the 
first  indication  of  the  division  of  the  atrium  into  right  and  left 
chambers  which  are  later  completely  separated  from  each 
other.  At  the  same  time  a  sHght  longitudinal  groove  appears 
in  the  surface  of  the  ventricle  (Fig.  49,  L,  i.v.)  which  indicates 
the  beginning  of  the  separation  of  the  ventricle  into  right  and 
left  chambers.     The  division  of  the  bulbo-conus  to  form  the 


142 


EARLY  EMBRYOLOGY   OF   THE   CHICK 


root  of  the  adrta  and  the  pulmonary  artery  does  not  appear 
until  a  later  stage  of  development. 

During  the  changes  in  the  external  shape  of  the  heart  which 
have  been  described,  the  whole  heart  has  come  to  occupy  a 
more  caudal  position  with  reference  to  other  structures  in  the 


M  lomitc* 


Pig.  49. — Ventral  views  of  the  heart  at  various  stages  to  show  its  changes 
of  shape  and  its  regional  differentiation.  All  the  drawings  were  made  from 
dissections  with  the  aid  of  camera  lucida  outlines.  The  outer  of  the  two  layers 
shown  is  the  epi-myocardium ;  the  inner,  the  endocardium.  In  the  stages  repre- 
sented in  Figs.  E-H  torsion  of  the  embryo's  body  is  going  on  at  the  level  of  the 
heart.  Since  torsion  involves  the  more  cephalic  regions  first  and  progresses 
caudad  the  transverse  axis  of  the  body  of  the  embryo  is  at  different  inclinations 
to  the  yolk  at  the  cephalic  end  and  at  the  caudal  end  of  the  heart.  In  drawing 
these  figures  their  orientation  was  taken  from  the  body  at  the  level  of  the  conus 
region  of  the  heart,  the  sinus  region  therefore  appears  inclined.  Abbreviations: 
a.v.,  constriction  between  atrium  and  ventricle;  i.v.,  interventricular  groove. 


embryo.     When  the  heart  is  first  formed  it  lies  at  the  level  of 
the  rhombencephalon.     As  development  progresses  it  moves 


STRUCTURE    OF   FOUR-DAY   CHICKS 


143 


farther  and  farther  caudad  until  at  the  end  of  the  fourth  day 
it  Hes  at  the  level  of  the  anterior  appendage  buds.  Being  un- 
attached to  the  body,  the  ventricular  region  of  the  heart  is 
carried  farthest  caudad  (Cf.  Figs.  19,  29,  34,  and  40). 

The  changes  which  take  place  in  the  heart  wall  can  be  seen 
best  in  sections.     The  endocardium  in  the  heart  of  a  four-day 


D38t 
16  I 


K 


76    HOVtS 
3t     tomitct 


Fig.  50. — Dextral  views  of  the  same  series  of  hearts  shown  in  ventral  view 
in  Pig.  49.  The  heart  drawings  in  Figs.  49  and  50  should  be  compared  with 
actual  specimens  or  with  drawings  of  entire  embryos  of  corresponding  age  for 
the  relation  of  the  heart  to  the  body  of  the  embryo. 

chick  is  still  a  single  cell  layer  lining  the  lumen.  The  original 
epi-myocardium  at  this  stage  can  be  differentiated  into  an 
inner  myocardial  portion  and  an  outer  epicardial  portion.  The 
myocardium  has  become  greatly  thickened  and  the  cells  in  it 
are  elongated  and  beginning  to  show  the  histological  character- 


144  EARLY   EMBRYOLOGY    OF   THE    CHICK 

istics  of  developing  muscle  cells.  Their  arrangement  in  bun- 
dles which  project  toward  the  lumen  fore-shadows  the  formation 
of  the  muscle  bands  (trabeculae  carneae)  which  ridge  the  inner 
wall  of  the  adult  heart.  The  cells  of  the  epicardial  portion  of 
tlie  epi-myocardium  are  becoming  flattened  to  form  the  epi- 
thelial and  connective  tissue  covering  of  the  heart  (epicardium) . 
Lying  between  the  endocardium  and  the  myocardium  in  the 
region  of  the  atrio- ventricular  canal  and  of  the  opening  of  the 
ventricle  into  the  bulbo-conus,  there  are  loosely  aggregated 
cells  which  are  mesenchymal  in  characteristics.  These  cells 
constitute  what  is  called  endocardial  cushion  tissue.  They 
later  take  part  in  the  formation  of  the  septa  which  divide  the 
heart  into  chambers  and  in  the  formation  of  the  connective 
tissue  frame-work  of  the  cardiac  valves. 

VI.  The  Urinary  System 

The  General  Relationships  of  Pronephros,  Mesonephros 
and  Metanephros. — In  the  development  of  the  urinary  system 
of  birds  and  mammals  there  are  formed  in  succession  three  dis- 
tinct excretory  organs,  pronephros,  mesonephros,  and  meta- 
nephros. The  pronephros  is  the  most  anterior  of  the  three, 
and  the  first  to  be  formed.  It  is  wholly  vestigial,  appearing 
only  as  a  slurred-over  recapitulation  of  structural  conditions 
which  exist  in  the  adults  of  the  most  primitive  of  the  vertebrate 
stock.  The  mesonephros  is  homologous  with  the  adult  excre- 
tory organs  of  fishes  and  amphibia.  It  makes  its  appearance 
in  the  embryo  somewhat  later  than  the  pronephros,  and  is 
formed  caudal  to  it.  The  mesonephros  is  the  principal  organ 
of  excretion  during  early  embryonic  life,  but  it  also  disappears 
in  the  adult  except  for  parts  of  its  duct  system  which  become 
associated  with  the  reproductive  organs.  The  metanephros 
is  the  most  caudally  located  of  the  excretory  organs,  and  the 
last  to  appear.  It  becomes  functional  toward  the  end  of  em- 
bryonic life  when  the  mesonephros  is  disappearing,  and  per- 
sists permanently  as  the  functional  kidney  of  the  adult. 

Figure  51  shows  schematically  some  of  the  main  steps  in  the 
embryological  history  of  the  nephric  organs,  which  it  will  be 
helpful  to  have  in  mind  before  taking  up  in  detail  any  of  the 
phases  of  their  formation  in  the  chick.  The  pronephros,  meso- 
nephros and  metanephros  are  all  derived  from  the  intermediate 


STRUCTURE    OF    FOUR-DAY   CHICKS 


145 


mesoderm,  and  are  all  composed  of  units  which  are  tubular  in 
nature.  In  the  different  nephroi  these  tubules  vary  in  struc- 
tural detail  but  their  functional  significance  is  in  all  cases  much 
the  same.  They  are  concerned  in  collecting  waste  materials 
from  the  capillary  plexuses  which  are  developed  in  connection 
with  them.     In  the  accompanying  diagrams  conventionahzed 


fr- 


pronephric 

tubules 

pronephric  tubules 
(degenerating)     ^^ 

mesonephric 

1?? 

pronephric 

tubules  with 

l/^j^ 

duct 

nephrostomes 

/'^^^ 

—    mesonephric 
tubules 

mesonephric 

tubules  without 

nephrostom 

i 

mesonephric  duct 

I     li 

mesonephric  •=:>      i  j] 

tubules  ^"nv--  ; 

and  duct 
degenerating 


mesonephric  duct 
metanephric  duct 
cloaca 


Fig.  51. — Schematic  diagrams  to  show  the  relations  of  pronephros,  meso- 
nephros,  and  metanephros  at  various  stages  of  development.  For  explanation 
see  text. 


tubules  have  been  drawn  to  represent  the  three  nephric  organs. 
No  pretense  is  made  of  representing  either  the  exact  shape  or 
the  actual  number  of  the  tubules. 

In  the  first  stage  represented  (Fig.  51,  ^)  only  the  pronephros 
has  been  established.  It  consists  of  a  group  of  tubules  empty- 
ing into  a  common  duct,  called  the  pronephric  duct.     The  pro- 


10 


146  EARLY   EMBRYOLOGY   OF   THE   CHICK 

nephric  ducts  of  either  side  are  formed  first  at  the  level  of  the 
pronephric  tubules  and  then  extend  caudad,  eventually  reach- 
ing and  opening  into  the  cloaca  (See  arrows  in  Fig.  51,  A). 

As  the  pronephric  ducts  are  extended  caudal  to  the  level  at 
which  pronephric  tubules  are  formed  they  come  in  close  prox- 
imity to  the  developing  mesonephric  tubules.  In  their  growth 
the  mesonephric  tubules  extend  toward  the  pronephric  ducts 
and  soon  open  into  them  (Fig.  51,  B).  Meanwhile  the  pro- 
nephric tubules  begin  to  degenerate.  Thus  the  ducts  which 
originally  arose  in  connection  with  the  pronephros  are  appro- 
priated by  the  developing  mesonephros.  After  the  degenera- 
tion of  the  pronephric  tubules  these  same  ducts  are  called  the 
mesonephric  ducts  because  of  their  new  associations  (Fig.  51,  C). 

At  a  considerably  later  stage  outgrowths  develop  from 
the  mesonephric  ducts  near  their  cloacal  ends  (Fig.  51,  C). 
These  outgrowths  form  the  ducts  of  the  metanephroi.  They 
grow  cephalo-laterad  and  eveiitually  connect  with  the  third 
group  of  tubules  developed  from  the  intermediate  mesoderm, 
the  metanephric  tubules  (Fig.  5 1 ,  Z>) .  With  the  establishment 
of  the  metanephroi  or  permanent  kidneys  the  mesonephroi 
begin  to  degenerate.  The  only  parts  of  the  mesonephric 
system  to  persist,  except  in  vestigial  form,  are  some  of  the  ducts 
and  tubules  which  in  the  male  are  appropriated  by  the  testis 
as  a  duct  system. 

The  Pronephric  Tubules  of  the  Chick. — The  pronephros 
in  the  chick  is  represented  by  tubules  which  first  appear  at  about 
36  hours  of  incubation.  The  pronephric  tubules  arise  from  the 
intermediate  mesoderm,  or  nephrotome,  lateral  to  the  somites. 
They  are  paired,  segmen tally  arranged  structures,  a  tubule 
appearing  on  either  side  opposite  each  somite  from  the  fifth  to 
the  sixteenth.  Transverse  sections  passing  through  the  loth  to 
14th  somites  of  an  embryo  of  about  38  hours  show  the  proneph- 
ric tubules  favorably.  Each  tubule  arises  as  a  solid  bud  of  cells 
organized  from  the  intermediate  mesoderm  near  its  junction 
with  the  lateral  mesoderm  (Fig.  52,  ^).  At  first  the  free  ends 
of  the  buds  grow  dorsad,  passing  close  to  the  posterior  cardinal 
veins.  Later  the  end  of  each  tubule  is  bent  caudad  coming  in 
contact  with  the  tubule  lying  posterior  to  it.  In  this  manner 
the  distal  ends  of  the  tubules  give  rise  to  a  continuous  cord  of 
cells,  the  primordium  of  the  pronephric  duct.     The  pair  of  cell 


STRUCTURE  OF  FOUR-DAY  CHICKS 


147 


cords  thus  formed  continue  to  extend  caudad  beyond  the 
pronephric  tubules  and  soon  become  hollowed  out  to  form  open 
ducts.  When  they  eventually  reach  the  level  of  the  cloaca  they 
turn  ventrad  and  open  into  it. 

The  significance  of  the  rudimentary  structures  in  the  chick 
which  represent  pronephric  tubules,  can  be  most  readily 
understood  by  comparing  them  with  fully  developed  and  func- 
tional pronephric  tubules.     Figure  52,  B,  shows  the  scheme  of 


ntermediate 
mesoderm 


dorsal  aorta 

^  coelom 

,  notochord 

X  somite 

/^                dorsal  aorta 

v/^ 

post,  cardinal 

^^K       ^ 

^        vein 

k^\/^ 

^  mesonephric 

W^^^^ 

duct 

^^^ 

mesonephric 

<S^'^ 

tubule 

-1 ^-"^ 

~         nephrostome 

^^ 

coelom 

nephrostome 


glomus 


somite 

dorsal  aorta 


:$. 


nephrostome 
glomerulus 

Fig.  52. — Drawings  to  show  nephric  tubules.  A,  drawing  from  transverse 
section  through  twelfth  somite  of  i6  somite  chick  to  show  pronephric  tubule. 
(After  Lillie.)  B,  schematic  diagram  of  functional  pronephric  tubule.  {After 
Wiedersheim.)  C,  drawing  from  transverse  section  through  seventeenth  somite 
of  30-somite  chick,  to  show  primitive  mesonephric  tubule;  D,  schematic  diagram 
of  functional  mesonephric  tubule  of  primitive  type.  {After  Wiedersheim.) 
For  a  later  stage  of  the  mesonephric  tubules  of  the  chick  see  Fig.  53, 


organization  of  a  functional  pronephric  tubule.  The  ciHated 
nephrostome  draws  iij  fluid  from  the  coelom.  As  the  fluid  passes 
the  capillaries  of  the  glomus,  waste  materials  from  the  blood  are 
transferred  to  it.  The  nephric  duct  serves  to  collect  and 
discharge  the  fluid  passing  through  the  tubules.  Vestiges  of 
a  nephrostome  opening  into  the  coelom  appear  in  the  pronephric 
tubules  of  the  chick  (Fig.  5 2, A)  but  the  tubules  never  become 


148  EARLY  EMBRYOLOGY   OF   THE   CHICK 

completely  patent,  and  never  acquire  the  vascular  connections 
characteristic  of  the  functional  pronephros  in  primitive 
vertebrates. 

The  Mesonephric  Tubules. — The  mesonephric  tubules  de- 
velop from  the  intermediate  mesoderm  caudal  to  the  pronephros. 
The  early  steps  in  their  formation  are  well  shown  in  transverse 
sections  of  chicks  of  29  to  30  somites  (about  55  hours).  In 
the  posterior  somites  conditions  are  less  advanced  than  they 
are  more  anteriorly.  Consequently  by  studying  the  posterior 
sections  of  a  transverse  series  first  and  then  progressing  cephalad 
a  graded  series  of  developmental  stages  may  be  obtained. 

The  mesonephric  tubules  appear  first  as  cell  clusters  formed 
in  the  intermediate  mesoderm.  They  lie  ventro-mesial  to  the 
cord  of  cells  which  is  the  primordium  of  the  pronephric  duct. 
The  cells  of  the  developing  tubules  acquire  a  more  or  less  radial 
arrangement,  and  at  the  same  time  become  more  distinctly 
isolated  from  the  surrounding  mesoderm  cells.  By  55  hours  of 
incubation  the  primordial  cell  cord  representing  the  pronephric 
duct  has  become  hollowed  out  to  establish  a  definite  lumen. 
The  most  anterior  of  the  mesonephric  tubules  also  have 
acquired  a  lumen.  The  growth  of  the  tubules  brings  them  in 
close  association  with  the  duct.  In  some  of  the  more  differen- 
tiated tubules  indications  can  be  made  out  of  their  opening  into 
the  duct  which  is  soon  to  be  definitely  established.  The  more 
posterior  mesonephric  tubules  do  not  become  associated 
with  the  duct  until  somewhat  later,  but  remain  as  a  series  of 
isolated  vesicles. 

Figure  52,  Z),  shows  the  scheme  of  organization  of  a  functional 
mesonephric  tubule  of  primitive  type.  As  is  the  case  with  the 
pronephric  tubule,  its  ciliated  nephrostome  draws  in  fluid 
from  the  coelom.  The  mesonephric  tubule  differs  from  the 
pronephric  chiefly  in  its  relation  to  the  blood  vessels  associated 
with  it.  It  develops  a  cup-like  outgrowth  into  which  a  knot 
of  capillaries  is  pushed.  The  cup-shaped  outgrowth  from  the 
tubule  is  called  the  capsule  (of  Bowman)  and  the  tuft  of  capil- 
laries, a  glomerulus.  Waste-laden  fluid  is  extracted  from 
the  capillaries  of  the  glomerulus,  mingles  with  the  fluid  coming 
in  by  way  of  the  nephrostome.  and  is  eventually  discharged  into 
the  nephric  duct.  In  mesonephric  tubules  of  a  more  highly 
differentiated  type  the  nephrostome  becomes  closed  and  all  the 


STRUCTURE    OF   FOUR-DAY   CHICKS 


149 


fluid  passing  through  the  tubule  is  drawn  from  the  glomerulus 
and  other  capillaries  adjacent  to  the  tubule. 

In  the  chick  a  few  of  the  more  anterior  mesonephric  tubules 
are  of  the  primitive  type  and  show  vestiges  of  a  nephrostome 
opening  into  the  ccelom  (Fig.  52,  C).  These  anterior  meso- 
nephric tubules,  however,  persist  for  but  a  short  time,  do  not 
attain  the  characteristic  relation  to  a  glomerulus  and  never 
become  functional.  Even  in  chicks  of  four  days'  incubation 
the  mesonephric  tubules  have  not  attained  their  full  develop- 
ment.    It  is  possible,  however,   to  make  out  most  of  their 


post  cardinal  v.-v 
coelom 


jnesonephnc 
duct 


mesonephric 
tubule 

developing  capsule 
and  glomerulus 


mesentery 


Fig.   53. — Drawing  from  transverse  section  of  four-day  chick  to  show  meso- 
nephric tubule  and  duct.     For  the  location  of  the  area  drawn  consult  Fig.  46,  F, 

fundamental  parts  (Fig.  53).  The  tubules  lying  in  the  ven- 
tro-Iateral  portion  of  the  mesonephros  have  been  longest  estab- 
lished and  are  somewhat  more  advanced  in  development  than 
those  lying  in  the  dorso-mesial  portion.  Nearly  all  of  the 
tubules  have  become  elongated  and  somewhat  coiled.  At  one 
end  they  open  into  the  mesonephric  duct  or  a  diverticulum  of 
the  duct  which  acts  as  a  collecting  tubule.  At  their  other  end 
a  cluster  of  closely  packed  cells  indicates  the  place  at  which 
the  capsule  and  glomerulus  will  appear.  The  glomeruH  develop 
very  rapidly.  Circulation  is  usually  estabhshed  in  them  by 
the  fifth  day.     From  this  time  until  about  the  eleventh  day 


150  EARLY   EMBRYOLOGY    OF    THE    CHICK 

of  incubation  the  functional  activity  of  the  mesonephros  is  at 
its  height.  After  the  eleventh  day  the  developing  metanephros 
begins  to  become  active  and  the  mesonephros  degenerates. 
The  establishment  of  the  metanephros  and  the  development 
of  the  genital  organs  occur  in  stages  which  are  too  advanced 
to  come  within  the  scope  of  this  book. 

VII.  The  Ccelom  and  Mesenteries 

In  a^^lt  birds  and  mammals  the  body  cavity  consists  of  three 
regions,  pericardial,  pleural  and-pmtOJieaL  The  pleural  divi- 
sion is  paired,  each  of  the  pleural  chambers  being  a  laterally 
situated  sac  containing  one  of  the  lungs.  The  pericardial 
chamber  containing  the  heart,  and  the  peritoneal  chamber  con- 
taining the  viscera,  other  than  the  lungs  and  heart,  are  un- 
paired. These  regions  of  the  adult  body  cavity  are  formed  by 
the  partitioning  off  of  the  primary  body  cavity  or  coelom  of 
the  embryo. 

In  the  chick  the  coelom  arises  by  a  splitting  of  the  lateral 
mesoderm  of  either  side  of  the  body  (Fig.  54,  A,  B).  It  is 
therefore,  primarily  a  paired  cavity.  Unlike  the  coelom  of 
some  of  the  more  primitive  vertebrates,  the  coelom  of  the  chick 
never  shows  any  indications  of  segmental  pouches  correspond- 
ing in  arrangement  with  the  somites.  The  right  and  left 
coelomic  chambers  extend  antero-posteriorly  without  interrup- 
tion through  the  entire  lateral  plates  of  mesoderm.  This  dif- 
ference in  the  formation  of  the  coelom  does  not  imply  any  lack 
of  homology  between  the  coelom  of  the  chick  and  that  of  more 
primitive  forms.  The  process  of  coelom  formation  in  the  chick 
may  be  considered  as  being  accelerated  with  a  resultant  slur- 
ring over  of  the  early  phases.  The  coelom  first  appears  in  a 
condition  which  is  comparable  with  the  coelom  of  more  primi- 
tive forms  at  that  period  of  differentiation  when  the  segmen- 
tally  arranged  coelomic  pouches  have  broken  through  into  each 
other  and  their  cavities  have  become  confluent. 

The  coelomic  chambers  are  not  limited  to  the  region  in  which 
the  body  of  the  embryo  is  developing.  They  extend  on  either 
side  into  the  mesoderm,  which  in  common  with  the  other  germ 
layers,  spreads  out  over  the  yolk  surface.  A  large  part  of  the 
primitive  coelomic  chambers  thus  comes  to  be  extra-embryonic 


STRUCTURE    OF   FOUR-DAY   CHICKS 


151 


in  its  associations.  (See  Chapter  XI  and  Figures  30  and  32.) 
The  portion  of  the  coelom  which  gives  rise  to  the  embryonic 
body  cavities  is  first  marked  off  by  the  series  of  folds  which 


A 
B 
C 


neural  plate 
notochord 
entoderm 


dorsal  mesoderm 

intermediate  mesoderm 
lateral  mesoderm 


splanchnopleure 


dorsal  aorta 
somatopleure 


ntermediate  mesoderm 

somatic  mesoderm 


splanchnic  mesoderm 


splanchnopleure 


mtermediate  mesoderm 

embryonic  coelom 
lateral  body  fold 


extra-embryonic 
coelom 


dorsal  aorta 
post,  cardinal  v 

mesenchyme 

somatopleure 
splanchnopleure  r^r^^ 


mesonephric  duct  and  tubule 

(from  intermediate  mesoderm) 
lateral  amniotic   fold 

intra-embryonic  coelom 
extra-embryonic    coelom 


liver   in 

ventral    • 
mesentery 


right  and  left 
coelom  confluent 


Fig.  54. — Schematic  diagrams  of  cross  sections  at  various  stages  to  show  the 
establishment  of  the  coelom  and  mesenteries.     For  explanation  see  text. 


separate  the  body  of  the  embryo  from  the  yolk  (Fig.  54,  C,  D) . 
As  the  closure  of  the  ventral  body  wall  progresses  (Fig.  54, 
E,  F)  the  embryonic  coelom  becomes  completely  separated  from 


152  EARLY  EMBRYOLOGY   OF   THE   CHICK 

the  extra-embryonic.  The  delayed  closure  of  the  ventral  body 
wall  in  the  yolk-stalk  region,  results  in  the  embryonic  and 
extra-embryonic  ccelom  retaining  their  open  communication  at 
this  point  for  a  long  time  after  they  have  been  completely 
separated  elsewhere. 

The  same  folding  process  which  establishes  the  ventral 
body  wall  completes  the  gut  ventrally  (Fig.  54,  C  to  F) .  Mean- 
while the  right  and  left  ccelomic  chambers  are  expanded  mesiad. 
As  a  result  the  newly  closed  gut  comes  to  He  suspended  between 
the  two  layers  of  splanchnic  mesoderm  which  constitute  the 
mesial  walls  of  the  right  and  left  ccelomic  chambers,  respec- 
tively. The  double  layers  of  splanchnic  mesoderm  which  thus 
become  apposed  to  the  gut  and  support  it  in  the  body  cavity 
are  known  as  mesenteries.  The  mesentery  dorsal  to  the  gut, 
suspending  it  from  the  dorsal  body  wall  is  the  primary  dorsal 
mesentery,  and  that  ventral  to  the  gut,  attaching  it  to  the  ven- 
tral body  wall  is  the  primary  ventral  mesentery. 

When  the  dorsal  and  ventral  mesenteries  are  first  established 
they  constitute  a  complete  membranous  partition  dividing  the 
body  cavity  into  right  and  left  halves.  The  primary  dorsal 
mesentery  persists  in  large  part  but  the  ventral  mesentery  early 
disappears  bringing  the  right  and  left  ccelomic  chambers  into 
confluence  ventral  to  the  gut  and  establishing  the  unpaired 
condition  of  the  body  cavity  characteristic  of  the  adult. 

In  considering  the  early  development  of  the  heart  (Chapter 
IX)  the  formation  of  the  dorsal  and  ventral  mesocardia  was 
taken  up.  In  their  relation  to  the  other  mesenteries  of  the 
body,  the  inesocardia  are  to  be  regarded  as  special  regions  of  the 
primary  ventral  mesentery.  In  the  most  cephalic  part  of  the 
body  cavity,  the  gut  lies  embedded  in  the  dorsal  body  wall 
instead  of  being  suspended  by  the  primary  dorsal  mesentery  as 
it  is  farther  caudally  (Cf.  Fig.  26,  E  and  Fig.  54,  F).  The 
ventral  mesentery  is,  however,  developed  in  the  same  manner 
anteriorly  as  it  is  posteriorly  and  when  the  heart  is  formed  it  is 
suspended  in  the  most  anterior  part  of  the  primary  ventral 
mesentery.  The  dorsal  and  ventral  mesocardia  are  the  parts 
of  the  primary  ventral  mesentery  lying  dorsal  to  the  heart,  and 
ventral  to  the  heart,  respectively  (Fig.  26,  D). 

When  the  ventral  mesocardium,  and  a  little  later  the  dorsal 
mesocardium,  breaks  through,  the  primary  right  and  left  coe- 


STRUCTURE    OF   FOUR-DAY   CHICKS 


153 


lomic  chambers  become  confluent  to  form  the  pericardial 
region  of  the  body  cavity  (Figs.  24  and  55).  Later  in  develop- 
ment the  ventral  mesentery  farther  caudally  disappears  so  that 
caudally  as  well  as  cephalically  an  unpaired  condition  of  the 
coelom  is  brought  about  (Fig.  54,  H). 

In  the  liver  region  the  ventral  mesentery  does  not  disappear. 
The  liver  arises  as  an  outgrowth  from  the  gut  and  in  its  develop- 
ment extends  into  the  ventral  mesentery  (Fig.  54,  G).  The 
portion  of  the  ventral  mesentery  dorsal  to  the  liver  persists  as 


ventral  pancreas 
dorsal  pancreas 


astro- hepatic  omentum 
stomach 


large  intestine 


(pericardial 
region) 


allantoic  stalk 


coelom 
(peritoneal  region) 


Pig.  55. — Schematic  lateral  view  of  dissection  of  four-day  chick  to  show  the  body 
cavity  and  the  more  important  mesenteries. 


the  gastro-hepatic  omentum,  and  the  portion  ventral  to  the 
liver   persists    as    its   ventral   ligament    (falciform     ligament) 

(Fig.  55)-^ 

The  primary  dorsal  mesentery  persists  and  forms  the  sup- 
porting membranes  of  the  digestive  tube.  In  the  adult  its 
different  regions  are  named  according  to  the  parts  of  the  digest- 
ive tube  with  which  they  are  associated,  as  for  example,  meso- 
gaster  that  part  of  the  primary  dorsal  mesentery  which  suspends 
the  stomach,  mesocolon,  that  part  of  the  primary  dorsal  mesen- 
tery supporting  the  colon,  etc. 

The  separation  of  the  body  cavity  into  pericardial,  pleural, 
and  peritoneal  chambers  is  accomplished  by  the  formation  of 


154  EARLY   EMBRYOLOGY   OF   THE    CHICK 

septa  growing  in  from  the  body  wall.  Consideration  of  the 
details  of  their  formation  would  lead  us  into  stages  of  develop- 
ment beyond  the  scope  of  this  book.  Those  interested  in 
following  the  later  embryology  of  the  chick  will  find  in  the 
appendix  references  to  more  exhaustive  books,  and  to  a  few  of 
the  more  recent  original  papers  on  its  development. 


APPENDIX 

REFERENCES  FOR  COLLATERAL  READING 

For  a  comprehensive  Bibliography  of  the  subject  reference 
should  be  made  to  Minot  (1893)  and  to  LilHe  (1908).  The 
references  given  here  have  been  selected  as  representative  of  the 
original  work  which  has  been  done  in  various  parts  of  the  field. 
By  placing  before  the  student  references  to  a  few  of  the  more 
readily  accessible  articles  it  is  hoped  to  encourage  him  to  do 
collateral  reading  of  original  papers  on  subjects  which  arouse 
his  interest. 

General  Development  of  the  Chick 

Duval,  M.,  1889.     Atlas  d'embryologie.    Masson,  Paris.     116  pp.,  40  plates. 

Foster,  M.,  and  Balfour,  F,  M.,  1883.  The  Elements  of  Embryology,  Part  I. 
The  History  of  the  Chick.  Macmillan,  London  and  New  York.  Second  Edi- 
tion, xiv  +  486  pp. 

Her  twig,  O.,  1 901- 190  7.  Handbuch  der  Vergleichenden  und  Experimentellen 
Entwickelungslehre  der  Wirbeltiere.  (Edited  by  Hertwig,  written  by  numerous 
collaborators.)     Fischer,  Jena. 

Kaupp,  B.  F.,  1918.  The  Anatomy  of  the  Domestic  Fowl.  Saunders, 
Philadelphia  and  London,  37 s  PP- 

Keibel,  F.,  and  Abraham,  K.,  1900.  Normaltafeln  zur  Entwickelungs- 
geschichte  des  Huhnes  (Gallus  domesticus).     Fischer,  Jesna.     132  pp.,  3  plates. 

Kellicott,  W.  E.,  1913.  Outlines  of  Chordate  Development.  Holt,  New 
York.     V  -|-  471  pp. 

Kerr,  J.  G.,  1919.  Textbook  of  Embryology.  Vol.  II.  Vertebrata  with  the 
Exception  of  Mammalia.     Macmillan,  London  and  New  York,    xii  +591  pp. 

Lillie,  F.  R.,  1908.  The  Development  of  the  Chick.  Holt,  New  York. 
Second  Edition,  1919.     xi  +  472  pp. 

Marshall,  A.  M.,  1893.  Vertebrate  Embryology.  (Chap.  IV,  The  Develop- 
ment of  the  Chick.)     Putnam,  New  York  and  London,    xxiii  +  640  pp. 

Minot,  C.  S.,  1893.  A  Bibliography  of  Vertebrate  Embryology.  Memoirs, 
Boston  Soc.  Nat.  History,  Vol.  IV,  Number  XI,  pp.  487-614. 

Minot,  C.  S.,  1903.  Laboratory  Text  Book  of  Embryology.  Blakiston's 
Son,  Philadelphia.     Second  Edition,  191 1.     xii  +  402  pp. 

Waite,  F.  C,  and  Patten,  B.  M.,  1918.  An  Outline  of  Laboratory  Work  in 
Vertebrate  Embryology.     Part  I.     The  Chick.     Judson,  Cleveland.     27  pp. 

Gametogenesis  and  Fertilization 

Bartelmez,  G.  W.,  19 12.  The  Bilaterality  of  the  Pigeon's  Egg.  A  Study  in 
Egg  Organization  from  the  First  Growth  Period  of  the  Oocyte  to  the  Beginning 
of  Cleavage.    Jour,  of  Morph.,  Vol.  23,  pp.  269-328. 

Firket,  Jean,  1920.  On  the  Origin  of  Germ-cells  in  Higher  Vertebrates. 
Anat.  Rec,  Vol.  18,  No.  3. 

155 


156  EARLY   EMBRYOLOGY   OF    THE   CHICK 

Guyer,  M.,  1909.  The  Spermatogenesis  of  the  Domestic  Chicken.  Ant. 
Anz.,  Bd.  34,  pp.  573-580. 

Harper,  E.  H.,  1904.  The  Fertilization  and  Early  Development  of  the 
Pigeon's  Egg.     Am.  Jour.  Anat.,  Vol.  Ill,  pp.  349-386. 

Kellicott,  W.  E.,  1913.  A  Text-book  of  General  Embryology.  Holt,  New 
York.    V  +  376  pp. 

Marshall,  F.  H.  A.,  1910.  The  Physiology  of  Reproduction.  Longmans, 
Green,  London,    xvii  +  706  pp. 

Pearl  R.,  and  Curtis,  M.  R.,  191 2.  Studies  on  the  Physiology  of  Reproduction 
in  the  Domestic  Fowl.  V.  Data  Regarding  the  Physiology  of  the  Oviduct. 
Jour.  Exp.  Zool.,  Vol.  12,  pp.  99-132. 

Riddle,  0.,  191 1.  On  the  Formation,  Significance  and  Chemistry  of  the 
White  and  Yellow  Yolk  of  Ova.    Jour.  Morph.,  Vol.  22,  pp.  455-492. 

Swift,  C.  H.,  1914.  Origin  and  Early  History  of  the  Primordial  Germ-cells 
in  the  Chick.     Am.  Jour.  Anat.,  Vol.  15,  pp.  483-516. 

Swift,  C.  H.,  1915.  Origin  of  the  Definitive  Sex-cells  in  the  Female  Chick 
and  Their  Relation  to  the  Primordial  Germ-cells.  Am.  Jour.  Anat.,  Vol.  18, 
pp.  441-470. 

Swift,  C.  H.,  1916.  Origin  of  the  Sex-cords  and  Definitive  Spermatogonia  in 
the  Male  Chick.     Am.  Jour.  Anat.,  Vol.  20,  pp.  375-410. 

Cleavage,  Gastrulation,  Genn -layer  Formation,  and  the  Early  Dififerentiation 

of  the  Embryo 

Bartelmez,  G.  W.,  1918.  The  Relation  of  the  Embryo  to  the  Principal 
Axis  of  Symmetry  in  the  Bird's  Egg.     Biol.  Bull.,  Vol.  35,  pp.  319-361. 

Blount,  M.,  1907.  The  Early  Development  of  the  Pigeon's  Egg,  with  Especial 
Reference  to  the  Supernumerary  Sperm  Nuclei,  the  Periblast,  and  the  Germ-wall. 
Biol.  Bull.,  Vol.  XIII,  pp.  231-250. 

Edwards,  C.  L.,  1902.  The  Physiological  Zero  and  the  Index  of  Development 
for  the  Egg  of  the  Domestic  Fowl.     Am.  Jour.  Physiol.,  Vol.  VI,  pp.  351-397. 

Eycleshymer,  A.  C,  1907.  Some  Observations  and  Experiments  on  the 
Natural  and  Artificial  Incubation  of  the  Egg  of  the  Conmion  Fowl.  Biol.  Bull., 
Vol.  XIII,  pp.  360-374. 

Hubbard,  M.  E.,  1908.  Some  Experinients  on  the  Order  of  Succession  of 
the  Somites  of  the  Chick.     Am.  Nat.,  Vol.  42,  pp.  466-471. 

Lewis,  Warren  H.  and  Lewis,  Margaret  R.,  1912.  The  Cultivation  of  Chick 
Tissues  in  Media  of  Known  Chemical  Constitution.  Anat.  Rec,  Vol.  6,  pp. 
207-212. 

McWhorter,  J.  E.,  and  Whipple,  A.  C,  191 2.  The  Development  of  the 
Blastoderm  of  the  Chick  in  Vitrio.     Anat.  Rec,  Vol.  6,  pp.  1 21-140. 

Patterson,  J.  T.,  1907.  The  Order  of  Appearance  of  the  Anterior  Somites  in 
the  Chick.     Biol.  Bull.,  Vol.  XIII,  pp.  1 21-133. 

Patterson,  J.  T.,  1909.  Gastrulation  in  the  Pigeon's  Egg;  a  Morphological  and 
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Patterson,  J.  T.,  1910.  Studies  on  the  Early  Development  of  the  Hen's  Egg. 
I.  History  of  the  Early  Cleavage  and  of  the  Accessory  Cleavage.  Jour,  of 
Morph.,  Vol.  21,  pp.  101-134. 

Peebles,  F.,  1904.  The  Location  of  the  Chick  Embryo  upon  the  Blastoderm. 
Jour.  Exp.  Z06I.,  Vol.  I,  pp.  369-384. 

Piatt,  J.  B.,  1889.  Studies  on  the  Primitive  Axial  Segmentation  of  the  Chick. 
Bull.  Mus.  Comp.  Zool.  Harv.,  Vol.  17. 


APPENDIX  157 

The  Nervous  System  and  Sense  Organs 

Abel,  W.,  191 2.  Further  Observations  on  the  Development  of  the  Sympa- 
thetic Nervous  System  in  the  Chick.  Jour.  Anat.  and  Physiol.,  Vol.  47,  pp. 
35-72. 

Beard,  J.,  1888.  Morphological  Studies,  II.  The  Development  of  the 
Nerv^ous  System  of  Vertebrates,  Pt.  I.  Elasmobranchs  and  Aves.  Quar. 
Jour.  Micr.  Sc,  Vol.  XXIX,  pp.  153-228. 

Cajal,  S.  R.  y.,.1889.  Sur  la  morphologie  et  les  connexions  des  Elements  de 
la  retine  des  oiseaux.     Anat.  Anz.,  Bd.  IV,  pp.  111-121. 

Cajal,  S.  R.  y.,  1890.  Sur  I'origine  et  le  ramifications  des  fibres  nerveuses  de 
la  moelle  embryonnaire.     Anat.  Anz.,  Bd.  V,  pp.  85-95  a-nd  111-119. 

Carpenter,  F.  W.,  1906.  The  Development  of  the  Oculomotor  Nerve,  the 
Ciliary  Ganglion,  and  the  Abducent  Nerve  in  the  Chick.  Bull.  Mus.  Comp. 
Zool.  Harv.,  Vol.  XL VIII. 

Cohn,  F.,  1903.  Zur  entwickelungsgeschichte  des  Geruchsorgans  des  Hiinch-' 
ens.     Arch.  mikr.  Anat.  u.  Entw.,  Bd.  LXE,  pp.  133-150. 

Cowdry,  E.  V.,  1914.  The  Development  of  the  Cytoplasmic  Constituents 
of  the  Nerve  Cells  of  the  Chick.     Am.  Jour.  Anat.,  Vol.  15,  pp.  389-430. 

Hill,  C,  1900.  Developmental  History  of  the  Primary  Segments  of  the 
Vertebrate  Head.     Zool.  Jahrbiicher,  Abth.  Anat.,  Bd.  XIII. 

Kupffer,  K.  v.,  1905.  Die  Morphogenie  des  Central  nervensystems.  Hert- 
wig's  Handbuch,  etc.,  Bd.  II,  Teil  3,  K.  VIII. 

Lewis,  W.  H.,  1903.  Wandering  Pigmented  Cells  Arising  from  the  Epithelium 
of  the  Optic  Cup,  with  Observations  on  the  Origin  of  the  M.  Sphincter  Pupillae 
in  the  Chick.     Am.  Jour.  Anat.,  Vol.  2,  pp.  405-416. 

Marshall,  A.  M.,  1878.  The  Development  of  the  Cranial  Nerves  in  the 
Chick.     Quar.  Jour.  Micr.  Sc,  Vol.  XVIII. 

Retzius,  G.,  1881-1884.  Das  Gehororgan  der  Wirbelthiere.  II.  Theil, 
Reptilien,  Vogel,  Sanger.     Stockholm. 

Weysse,  A.  W.,  and  Burgess,  W.  S.,  1906.  Histogenesis  of  the  Retina.  Am. 
Naturalist,  Vol.  XL,  pp.  611-638. 

The  Circulatory  System 

Boas,  J.  E.  v.,  1887.  Ueber  die  Arterienbogen  der  Wirbeltiere.  Morph. 
Jahrb.,  Bd.  XIII,  pp.  115-118. 

Chapman,  W.  B.,  1918.  The  Effect  of  the  Heart-beat  upon  the  Development 
of  the  Vascular  System  in  the  Chick.     Am.  Jour.  Anat.,  Vol.  23,  pp.  175-203. 

Clark,  Eleanor  Linton,  191 5.  Observations  on  the  Lymph  Flow  and  the 
Associated  Morphological  Changes  in  the  Early  Superficial  Lymphatics  of  Chick 
Embryos.     Am.  Jour.  Anat.,  Vol.  18,  pp.  399-440. 

Evans,  H.  M.,  1909.  On  the  Development  of  the  Aortae,  Cardinal  and 
Umbilical  Veins  and  other  Blood-vessels  of  Vertebrate  Embryos  from  Capillaries. 
Anat.  Record,  Vol.  3,  pp.  498-518. 

Greil,  A.,  1903.  Beitrage  zur  vergleichenden  Anatomie  und  Entwicklungs- 
geschichte  des  Herzens  und  des  Truncus  arteriosus  der  Wirbelthiere.  Morph. 
Jahrb.,  Vol.  31,  pp.  123-310. 

Hochstetter,  F.,  1906.  Die  Entwickelung  des  Blutgefasssystems.  Hertwig's 
Handbuch,  etc.,  Bd.  Ill,  Teil  2. 

Locy,  W.  A.,  1906.  The  Fifth  and  Sixth  Aortic  Arches  in  Chick  Embryos 
with  Comments  on  the  Condition  of  the  Same  Vessels  in  other  Vertebrates. 
Anat.  Anz.,  Bd.  XXIX,  pp.  287-300. 


158  EARLY   EMBRYOLOGY    OF    THE    CHICK 

Mackay,  J.  Y.,  1888.  The  Development  of  the  Branchial  Arterial  Arches 
in  Birds,  with  Special  Reference  to  the  Origin  of  the  Subclavians  and  Carotids. 
Phil.  Trans.  Roy.  Soc.  London,  Vol.  179,  Ser.  B,  pp.  111-139. 

Masius,  J.,  1889.  Quelques  notes  sur  le  developpement  du  coeur  chez  le  poulet. 
Arch.  Biol.,  T.  IX, pp. 403-41 8. 

Miller,  A.  M.,  1903.  The  Development  of  the  Postcaval  Vein  in  Birds.  Am. 
Jour.  Anat.,  Vol.  2,  pp.  283-298. 

Miller,  A.  M.,  and  McWhorter,  J.  E.,  1914.  Experiments  on  the  Develop- 
ment of  Blood  Vessels  in  the  Area  Pellucida  and  Embryonic  Body  of  the  Chick 
Anat.  Rec,  Vol.  8,  pp.  203-227. 

Patterson,  J.  T.,  1909.  An  Experimental  Study  on  the  Development  of  the 
Vascular  Area  of  the  Chick  Blastoderm.     Biol.  Bull.,  Vol.  16,  pp.  83-90. 

Sabine,  Florence  R.,  191 7.  Preliminary  Note  on  the  Differentiation  of 
Angioblasts  and  the  Method  by  which  they  Produce  Blood-vessels,  Blood- 
plasma  and  Red  Blood-cells  as  seen  in  the  Living  Chick.  Anat.  Rec,  Vol.  13, 
pp.  199-204. 

Stockard,  C.  R.,  1915.  An  Experimental  Analysis  of  the  Origin  of  Blood  and 
Vascular  Endothelium.     Memoirs  Wistar  Inst.  No.  7,  174  pp. 

Twining,  Granville  H.,  1906.  The  Embryonic  History  of  the  Carotid  Arteries 
in  the  Chick.     Anat.  Anz.,  Bd.  XXIX,  pp.  650-663. 

The  Digestive  and  Respiratory  Systems  and  the  Division  of  the  Body  Cavities 

Boyden,  Edward  A.,  191 8.  Vestigial  Gill  Filaments  in  Chick  Embryos 
with  a  Note  on  Similar  Structures  in  Reptiles.  Am.  Jour.  Anat.,  Vol.23,  pp. 
205-235. 

Brouha,  M.,  1898.  Recherches  sur  le  developpement  du  foie,  du  pancreas^ 
de  la  cloison  mesent6rique  et  des  cavities  hepato-enteriques  chez  les  oiseaux. 
Jour,  de  I'anat.  et  phys.,  T.  XXXIV. 

Butler,  G.  W.,  1889.  On  the  Subdivisions  of  the  Body-cavity  in  Lizards, 
Crocodiles,  and  Birds.     Proc.  Zool.  Soc.  London  for  1889,  pp.  452-474. 

Hammar,  G.  A.,  1897.  Ueber  einige  Hauptzuge  der  ersten  embryonalen 
Leberentwickelung.     Anat.  Anz.,  Bd.  XIII,  pp.  233-247. 

Lockward,  C.  B.,  1888.  The  Early  Development  of  the  Pericardium,  Dia- 
phragm and  Great  Veins.     Phil.  Trans.  Roy.  Soc.  London,  Vol.  CLXXIX,  B, 

pp.  365-384- 

Locy,  W.  A.,  and  Larsell,  O.,  1916.  The  Embryology  of  the  Bird's  Lung 
Based  on  Observations  of  the  Domestic  Fowl.  Am.  Jour.  Anat.,  Vol.  19,  pp. 
447-504  and  Vol.  20,  pp.  1-44. 

Mall,  F.  P.,  1 89 1.  Development  of  the  Lesser  Peritoneal  Cavity  in  Birds  and 
Mammals.    Jour.  Morph.,  Vol.  V,  pp.  165-179. 

Minot,  C.  S.,  1900.  On  the  Solid  Stage  of  the  Large  Intestine  in  the  Chick. 
Jour.  Bos.  Soc.  Med.  Sc,  Vol.  IV. 

Minot,  C.  S.,  1900.  On  a  Hitherto  Unrecognized  Form  of  Blood-circulation 
without  Capillaries  in  the  Organs  of  Vertebrata.  Proc.  Bos.  Soc.  of  Nat.  Hist, 
Vol.  XXIX,  pp.  185-215. 

Ravn,  E.,  1899.  Ueber  die  Entwickelung  des  Septum  Transversum,  Anat. 
.A.nz.,  Bd.  XV,  pp.  528-534. 

Schreiner,  K.  E.,  1900.  Beitrage  zur  Hitologie  und  Embryologie  des  Vorder- 
darms  der  Vogel.     Zeitschr.  wiss.  Zool.,  Bd.  LXVIII. 


APPENDIX  159 

The  Urinogenital  System 

Felix,  u.  BiJhler.,  1906.  Die  Entwickelung  der  Harn-  und  Geschlechts  organe. 
Hertwig's  Handbuch,  etc.,  Bd.  Ill,  Teil  I,  K.  II. 

Firket,  Jean,  1914.  Recherches  sur  I'organogen^se  des  glands  sexuelles  chez 
les  oiseaux.     Arch,  de  Biol.,  Tome  29,  pp.  201-351. 

Retterer,  E.,  1885.  Contribution  a  I'etude  du  cloaque  et  de  la  bourse  de 
Fabricius  chez  les  oiseaux.     Jour,  de  1'  anat.  et  de  la  phys.  XXI,  pp.  369-454. 

Sedgwick,  A.,  1880.  Development  of  the  Kidney  in  its  Relation  to  the 
Wolffian  Body  in  the  Chick.     Quart.  Jour.  Micr.  Sc,  Vol.  XX,  pp.  146-166. 

Sedgwick,  A.,  1881.  On  the  Early  Development  of  the  Anterior  Part  of  the 
Wolffian  Duct  and  Body  in  the  Chick  Together  with  Some  Remarks  on  the 
Excretory  System  of  Vertebra ta.     Quart.  Jour.  Micr.  Sc,  Vol.  XXI,  pp.  432-468. 

Schreiner,  K.  E.,  1902.  Ueber  die  Entwickelung  der  Amniotenniere.  Zeitschr. 
wiss.  Zool.,  Bd.  LXXI. 

The  Skeletal  and  Muscular  Systems 

Brachet,  A.,  1893.  Etude  sur  la  resorption  de  cartilage  et  le  developpement 
des  OS  longs  chez  les  oiseaux.     Internat.  Monatschr.  Anat.  und  Phys.,  Bd.  X. 

Engert,  H.,  1900.  Die  Entwickelung  der  ventralen  Rumpfmuskulatur  bei 
Vogeln.     Morph.  Jahrb.,  Bd.  XXIX,  pp.  169-185. 

Isaacs,  Raphael,  191 9.  The  Structure  and  Mechanics  of  Developing  Con- 
nective Tissue.     Anat.  Rec,  Vol.  17,  pp.  243-270. 

Johnson,  Alice,  1883.  On  the  Development  of  the  Pelvic  Girdle  and  Skeleton 
of  the  Hind  Limb  in  the  Chick.     Quar,  Jour.  Micr.  Sc,  Vol.  XXIIl. 

Kingsbury,  B.  F.,  1920.  The  Developmental  Origin  of  the  Notochord. 
Science,  N.  S.,  Vol.  51,  pp.  190-193. 

Parker,  W.  K.,  1869.  On  the  Structure  and  Development  of  the  Skull  of  the 
Common  Fowl  (Gallus  domesticus).  Phil.  Trans.  Roy.  Soc,  London,  Vol. 
CLIX,  Part  II,  pp.  755-807. 

Parker,  W.  K.,  1888.  On  the  Structure  and  Development  of  the  Wing  of  the 
Common  Fowl.     Phil.  Trans.  Roy.  Soc,  London,  Vol.  179,  Ser.  B,  pp.  385-398. 

Paterson,  A.  M.,  1888.  On  the  Fate  of  the  Muscle  Plate  and  the  Develop- 
ment of  the  Spinal  Nerves  and  Limb  Plexuses  in  Birds  and  Mammals.  Quart. 
Jour.  Mic.  Sci.,  Vol.  2S,  pp.  109-130. 

Williams,  L.  W.,  1910.  The  Somites  of  the  Chick.  Am.  Jour.  Anat.,  Vol. 
">  PP-  S5-IOO. 

Extra-embryonic  Membranes 

Danchakoff,  Vera,  191 7.  The  Position  of  the  Respiratory  Vascular  Net 
in  the  Allantois  of  the  Chick.     Am.  Jour.  Anat.,  Vol.  21,  pp.  407-420. 

Duval,  M.,  1884.  Etudes  histologiques  et  morphologiques  sur  les  annexes 
des  embryoAS  d'oiseaux.     Jour,  de  I'anat.  et  de  la  phys.,  T.  XX. 

Lillie,  F.  R.,  1903.  Experimental  Studies  on  the  Development  of  the  Organs 
in  the  Embryo  of  the  Fowl  (Gallus  domesticus).  i.  Experiments  on  the  Amnion 
and  the  Production  of  Anamiote  Embryos  of  the  Chick.  Biol.  Bull.,  Vol.  V, 
pp.  92-124. 

Popoff,  D.,  1894.     Die  Dottersackgefasse  des  Huhnes.     Wiesbaden. 

Shore,  T.  W.,  and  Pickering,  J.  W.,  1889.  The  Proamnion  and  Amnion  in  the 
Chick.     Jour,  of  Anat.  and  Phys.,  Vol.  XXIV,  pp.  1-2 1. 

Stuart,  T.  P.  A.,  1899.  A  Mode  of  Demonstrating  the  Developing  Membranes 
in  the  Chick.     Jour.  Anat.  and  Phys.,  Vol.  XXV,  pp.  299-300. 


l6o  EARLY   EMBRYOLOGY    OF   THE    CHICK 

The  Ductless  Glands 

Atwell,  W.  J.,  and  Si  tier,  Ida,  191 8.  The  Early  Appearance  of  the  Anlagen 
of  the  Pars  Tuberalis  in  the  Hypophysis  of  the  Chick.  Anat.  Rec,  Vol.  15, 
pp.  181-187. 

Poll,  H.,  1906.  Die  vergleichende  Entwickelungsgeschichte  der  Nebennieren 
systeme  der  Wlrbeltiere.  Hertwig,  O.,  Handbuch  der  Vergleichenden  und 
Experimentellen  Entwickelungslehre  der  Wirbeltiere.  (Edited  by  Hertwig, 
written  by  numerous  collaborators.)     Fischer,  Jena.     Bd.  Ill,  Teil  i,  K.  II,  2. 

Soulie,  A.  H.,  1903.  Recherches  sur  le  d^veloppement  des  capsules  surrenales 
chez  les  vert6br6s  superi^urs.  Jour,  de  I'anat.  et  physiol.,  T.  XXXIX,  pp. 
197-293. 

Verdun,  M.  P.,  1898.  Sur  les  d^riv^s  branchiaux  du  poulet.  Comptes  rendus 
See.  Biol.,  Tom.  V. 

Anomalies 

Alsop,  Florence  M.,  1919.  The  Effect  of  Abnormal  Temperatures  upon 
the  Developing  Nervous  System  in  the  Chick  Embryos.     Anat.  Rec,  Vol.  15, 

pp.  307-323- 

Glaser,  O.,  1913.  On  the  Origin  of  Double-yolked  Eggs.  Biol.  Bull.,  Vol, 
24,  pp.  175-186. 

Mitchell,  P.  C,  1891.  On  a  Double-chick  Embryo.  Jour,  of  Anat.  and 
Physiol.,  Vol.  25,  pp.  316-324. 

Pohlman,  A.  G.,  1920.  A  Consideration  of  the  Branchial  Arcades  in  Chick 
Based  on  the  Anomalous  Persistence  of  the  Fourth  Left  Arch  in  a  Sixteen-day 
Stage.    Anat.  Rec,  Vol.  18,  pp.  159-166. 

O'Donoghue,  C.  H.,  1910.  Three  Examples  of  Duplicity  in  Chick  Embryos 
with  a  Case  of  Ovum  in  Ovo.     Anat.  Anz.,  Bd.  37,  pp.  530-536. 

Stockard,  Charles  R.,  1914.  The  Artificial  Production  of  Eye  Abnormalities 
in  the  Chicken  Embryo.     Anat.  Rec,  Vol.  8,  pp.  33-42, 

Tannreuther,  G.  W.,  1919.  Partial  and  Complete  Duplicity  in  Chick  Em- 
bryos.    Anat.  Rec,  Vol.  16,  pp.  355-367. 


INDEX 

To  facilitate  the  use  of  this  book  in  connection  with  others  in  which  the  termi- 
nology may  dififer  somewhat,  many  synonyms  which  were  not  used  in  the  text 
have  been  put  into  the  index  and  cross-referenced  to  the  alternative  terms  used 
in  this  book.  For  example,  WolflSan  body,  a  term  not  used  in  this  text,  is  fre- 
quently applied  to  the  mesonephros.  It  appears  in  the  index  thus:  Wolflfian 
body  (=  mesonephros,  q.v.). 

Both  figure  and  page  references  are  given  in  the  index.  The  figure  references 
are  preceded  by  the  letter  f . 


Accessory  cleavage,  19 
Accessory  coverings  of  ovum,  f.  3,  10 
Acoustico-facialis  ganglion  (  =  gang- 
lion complex  of  VII  and  VIII 
cranial  nerves)  f.  40,  118 
Acoustic  ganglion,  f.  42,  118,  123 
Air  space,  f.  3,  12 
Albumen,  f.  3,  10 
Albumen-sac,  f.  30,  f.  32,  84,  87 
Alecithal  ovum  (see  isolecithal). 
Allantoic,  circulation  (see  circulation). 

diverticulum,  f.  $$,  90 

stalk,  f.  33,  f.  43,  90 

vesicle,  f.  30,  f.  32,  f.  33,  f.  40, 
90,  113 
Allan tois,  fate  of,  137 

formation  of,  f.  33,  90 

function  of,  90,  137 

relations  of,  f.  30,  f.  32 
Amnion,  formation,  f.  30,  f.  32, 86,  87 

fuaiction  of,  86 

muscle  fibers  of,  86 

relations  of,  f.  30,  f.  32 
Amnion,  false,  92 
Amnio-cardiac  vesicles,  49 
Amniotic,  cavity,  f.  30,  f.  32,  87 

fluid,  86 

folds,  f.  30,  f.  32,  87 

raphe,  87 
Anal  plate  (see  cloacal  membrane). 
Animal  pole,  8 

Anterior  horns  of  mesoderm,  f .  1 2 
Anterior  intestinal  portal,  f.  16,  f.  17, 

f.  31,  46,  57,  69 
Anterior  neuropore,  f.  19,  55,  99 


Aortas  dorsal,  formation  of,  73 

fusion  of,  105,  138 

position  of,  f.  23,  f.  24,  f.  35,  f.  47 
Aorta,  ventral,  f.  23,  f.  24,  f.  35,  f.  47, 

f.  73,-  los,  137 
Aortic  arches,  fate  of,  138 

formation  of,  105 

position  of,  f.  24,  f.  35,  f.  47 
Aortic  roots,  dorsal,  f.  34,  f.  47,  137 

ventral,  f.  23,  f.  35,  f.  47,  72,  137 
Appendage  buds,  anterior,  f.  39,  f.  40, 
112 

posterior,  f.  39,  f.  40,  112 
Aqueduct  of  Sylvius,  f.  42,  117 
Area  opaca,  f.  11,  f,  13,  24,  36 

vasculosa,  f.  15,  f.  17,  51 

vitellina,  f.  15,  f.  17,  51 
Area  pellucida,  f.  11,  f.  13,  24 
Area  vasculosa,  51,  58 
Arteries,  allantoic,  f.  47,  138 

aortic  (see  aorta) 

carotid,  ext.  f.  47,  137 

carotid,  int.  f.  47,  137 

coeliac,  139 

definition  of,  133 

iliac,  f.  47,  138 

mesenteric,  139 

omphalomesenteric,  f.  29,  f.  47, 
78,  los,  138 

pulmonary,  138 

segmental,  138 

sub-clavian,  138 

vitelline,  f.  48,  135 
Atrium,  f.  23,  f.  49,  f.  50,  72,  104,  141 
Atrio-ventricular  constriction,  f.  49, 141 


11 


161 


l62 


INDEX 


Auditory,     ganglion     (see    acoustic), 
nerve,  123 
pit,  f.  22,  65 
placode,  65,  122 
vesicle,  f.  36,  f.  40,  65,  122 

Bile  duct,  common,  126 
Blastocoele,  f.  6,  21,  23 
Blastoderm,  f.  6,  20,  24 

zones  of,  f.  7,  24 
Blastodisc,  16 
Blastomere,  16 
Blastopore,  f.  6,  22 

closure  of,  26 

concrescence  of,  f.  9,  28 

formation  of,  in  birds,  f .  7,  26 

homologies  of,  23 
Blastula,  20,  21,  24 
Blood,  as  a  carrier  of  food,  79,  132 

oxygenation  of,  78,  133 
Blood  cells,  origin  of,  f.  25,  66 
Blood  islands,  differentiation  of,  f.  25, 
66,67 

formation  of,  f ,  25,  51 

location  of,  f.  15,  f.  17 
Blood-vessels,     formation    of,    f.    25, 
66,  72  (see  also  arteries  and 
veins). 
Body  cavity  (see  coelom) , 
Body  folds,  f.  30,  f.  32,  80 
Bowman's  capsule,  148 
Brain,  first  differentiation  of,  53 

neuromeric  structure  of,  59 

primary  vesicles,  f .  20,  54,  60 

secondary  vesicles,  f.  42,  63,  114 

ventricles  of,  f.  42,  115 
Branchial  arches  (see  visceral  arches). 
Bulbo-conus  arteriosus,  f .   23 ,  f .  49, 

f.  50,  72,  141 
Bulbus   arteriosus   (see  bulbo-conus). 

Capsule  of  Bowman,  148 
Caudad,  usage  of  term,  5 
Caudal,  usage  of  term,  5 
Caudal  fold,  f.  31,  81 
Caudal  flexure,  1 1 1 
Central  canal  of  spinal  cord,  119 
Cephalad,  usage  of  term,  5 
Cephalic,  usage  of  term,  5 
Cephalic  limiting  fold,  80 
Cephalic  mesoderm,  40,  50 
Cephalic  neural  crest,  f.  22,  loi 


Cerebellar  peduncles,  118 

Cerebellum,  118 

Cerebral  ganglia  (see  ganglia,  cranial). 

Cerebral  hemispheres,  115 

Cervical  flexure,  94,  iii 

Chalaza,  f.  3,  10 

Chorion,  92 

Choroid  coat  of  eye,  122 

Choroid  fissure  of  eye,  f.  35,  f.  42,  98, 
121 

Choroid  plexus,  117,  118 

Circulation,  allantoic,  f.  47,  136 
course  of  embryonic,  78,  132 
establishment  of,  78 
intra-embryonic,  f.  47,  137 
significance  of  embryonic,  131 
vitelline,  f.  48,  68,  77,  134 

Cleavage,  accessory,  19 
discoidal,  f.  5,  16 
holoblastic,  f.  4,  16 
meroblastic,  f.  4,  16 
process  of,  in  birds,  f.  5,  16 

Cleavage  cavity  (see  blastocoele). 

Cloaca,  f.  31,  f.  43»  130 

Cloacal  membrane,  f.  31,  130 

Cloacal  opening,  130 

Coelom,  divisions  of  embryonic,  150 
extra-and  intra-embryonic,  f.  28, 

f.  30,  f.  32,  49,  151 
formation  of,  f,  54,  49>  150 
pericardial  region  of,  f.  16,  f.  24, 
f.  26,  f.  27,  49»  72,  ISO 

Concrescence,  of  blastopore,  f.  9,  28 
of  anterior  intestinal  portal,  69 

Conus  arteriosus  (see  bulbo-conus). 

Conjunctival  epithelium,  122 

Cornea,  122 

Corpora  quadrigemina,  117 

Corpus  vitreum  (see  vitreous  body). 

Cranial  flexure,  75,  11 1 

Crura  cerebri,  117 

Cutis  plate  (see  dermatome). 

Cystic  duct,  126 

Deutoplasm,  7 

effect  of  on  cleavage,  f .  4,  14 
effect  of  on  gastrulation,  f.  6,  21 

Dermatome,  f.  38,  f.  44,  107 

Diencephalon,  f.  42,  65,  116 

Diocoele   (=    lumen  of  diencephalon, 
q.  v.). 

Dio-mesencephalic  boundary,  f.  42, 117 


INDEX 


163 


Dio-telencephalic  boundary,  f.  42,  115 

Discoidal cleavage  (see  cleavage). 

Dorsad,  usage  of  term,  5 

Dorsal  aorta  (see  aorta). 

Dorsal  flexure,  in 

Dorsal  mesentery,  f.  54,  f.  55,  152 

Dorsal  mesocardium,  f.  26,  69,  71,  140, 

152 
Dorsal  nerve  roots,  f.  44,  119 
Dorsal  pancreatic  bud,  127 
Dorsal  root  ganglia,  f.  44,  119 
Dorsal,  usage  of  term,  5 
Duct  of  Cuvier  (=  common  cardinal 

vein,  q.  v.). 
Ductus  arteriosus  (part  of  aortic  arch 

VI). 
Ductus  choledochus,  f.  46  E.,  127 
Ductus  endo-lymphaticus,  f.  40,  122 
Ductus  venosus  (=  fused  portion  of 

omphalomesenteric    vein,   q. 

v.). 

Ear,  122 

Ectoderm,  derivatives  of,  31 

establishment  of,  23 
Egg,  membranes,  f.  3,  10 

ovarian,  f.  i,  7 

shell,  10,  12 

structure  of  at  lajdng,  f.  3,  11 
Embryo,  external  form  of,  93,  109 

separation   of   from   blastoderm, 
f.  30,  f.  32,  80 
Embryonal  area,  42 
Embryonic   circulation    (see     circula- 
tion). 
Endocardial  cushion  tissue,  f.  46  D,  144 
Endocardial  primordia,  f.  26,  f.  27,  69 
Endocardium,  143 
Endolymphatic  duct,  f.  40,  122 
Entoderm,  derivatives  of,  32 

establishment  of,  20,  23 
Endothelium,  origin  of  vascular,  f.  25, 

66 
Epicardium,  69,  143 
Epichordal  portion  of  brain,  55 
Epimyocardium,  fate  of,  140,  144 

formation  of,  f.  26,  f.  27,  69 
Epiphysis,  f.  35,  f.  42,  95,  116 
Eustachian  tube,  103,  123 
Extra-embryonic  ccelom  (see  coelom). 
Extra-embryonic    membranes,    f.    30, 
f.  32,  Chap.  XI 


Extra-embryonic  vascular  plexus  (see 
vitelline  circulation  and 
blood-vessels,  origin  of). 

Eye,  120 

Facial  region,  f.  41.  in 

Facial  nerve   (=  cranial  nerve  VII), 

118 
Falciform  ligament,  153 
Fertilization,  9 
Flexion,  75,  no 
Floor  plate  of  spinal  cord,  119 
Foramen  of  Monro,  f.  42,  114 
Follicle,  ovarian,  f.  i,  7 
Fore-brain  (see  prosencephalon). 
Fore-gut  (see  gut). 
Fovea  cardiaca  (=  anterior  intestinal 

portal  q.  v.). 
Frontal  process,  f.  41 

Gall  bladder,  126 

Gametes,  7 

Ganglia,  cranial,  f.  42,  118 

dorsal  root  (see  spinal). 

spinal,  f.  44,  119 

sympathetic,  f.  44,  120 
Ganglion    jugulare    (=    ganglion    of 

cranial  nerve  X.)  f.  42, 118 
Gasserian   ganglion    (=    ganglion   of 
cranial  nerve  V)  f.  40,   118 
Gastrocoele,  f,  6,  f.  7,  22,  26 
Gastro-hepatic  omentum,  153 
Gastrulation,  Chap.  IV 

effect  of  yolk  on,  f.  6,  21 

in  Amphioxus,  22 

in  Amphibia,  23 

in  birds,  f.  7,  24 
Geniculate  ganglion   (=    ganglion  of 
cranial  nerve  VII);   f.42,  118 
Germ  cells  (see  gametes). 
Germ  layers  (see  ectoderm,  entoderm 

and  mesoderm). 
Germinal  disc  (see  blastodisc). 
Germinal  epithelium  of  ovary,  f,  i 
Germinal  vesicle  ( =  nucleus  of  ovum, 

q.  v.). 
Germ  wall,  24 

Gill  arches  (see  visceral  arches). 
Glomerulus,  f.  52,  f.  53,  148 
Glomus,  f.  52 

Glossopharyngeal  nerve  (=  cranial 
nerve  IX),  f.  42, 118 


164 


INDEX     ' 


Glottis,  125 

Granular  zone  of  follicle,  8 
Gut,  delimitation  of  embryonic,  81 
fore-,  f.  17,  f.  31,  46,  57,  84,  loi 
hind-,  f.  31,  84,  102,  130 
mid-,  f.  31,  84,  102,  127 
pre-oral,  f.  31,  102,  124 
primitive,  f.  13,  f.  31,  36 
post-anal,  f.  31,  130 

Head  fold,  43,  80 
Head  fold  of  anmion,  f.  29,  86 
Head  process  (see  notochord). 
Heart,  differentiation  of,  f.  49,  f.  50, 
104, 139 

establishment  of  f.  26,  f.  27,  57,  68 

primordia  of,  50,  71 
Heart-beat,  72 

Hensen's  Node,  f.  8,  f.  11,  f.  13,  28 
Hepatic  duct,  126 
Hepatic-portal  circulation,  127 
Hepatic  tubules,  126 
Hind-brain    (see    rhombencephalon). 
Hind-gut  (see  gut). 
Holoblastic  cleavage  (see  cleavage). 
Homolecithal  ova  ( =  isolecithal,  q.  v.) . 
Hyoid  arch,  f.  39,  f.  41,  103 
Hyomandibular  cleft,  f.  34, 103, 123 
Hypophysis,  95,  117 

Incubation,  12 

Infundibulum,  f.  35,  f.  42,  f.  43,  63,  95, 
116 

Intermediate  mesoderm  (see  meso- 
derm). • 

Internal  ear,  123 

Interventricular  sulcus,  f.  49,  141 

Intestine,  127 

Intra-embryonic  ccelom  (see  coelom). 

Invagination  of  entoderm  (see  gastru- 
lation). 

Isolecithal  ova,  14 

Jugular  vein  (see  vein,  anterior  cardi- 
nal). 

Kidney  (see  metanephros). 

Lamina  terminalis,  f.  42,  114 
Latebra,  f.  3,  12 
Lateral  body  folds,  f.  30,  80 
Lateral  limiting  sulci  (=  lateral  body 
folds,  q.  V.) 


Lateral  mesoderm  (see  mesoderm). 
Lateral  plate  of  spinal  cord,  119 
Lateral    telencephalic    vesicles     (see 

telencephalon). 
Lateral  wings  or  horns  of  mesoderm,  f. 

12,  37 
Lens,  differentiation  of,  f.  45,  121 

fibers,  122 

origin  of,  98 

vesicle,  f.  36,  98 
Liver,  f.  43,  f.  46,  126 
Lung  buds,  f.  46,  125 

Mandibular  arch,  f.  36,  f.  4I;  103,  112 

Mandible,  112 

Marginal  notch,  f.  9 

Margin  of  overgrowth,  f.  7,  24 

Maturation  of  gametes,  9 

Maxilla,  112 

Maxillary  process,  f.  41,  112 

Meatus  venosus  (=  ductus  venosus, 

q.  v.). 
Medulla,  ji8 
Medullary    plate    (=    neural     plate, 

q.  v.). 
Meroblastic  cleavage  (see  cleavage). 
Mesencephalon,  f.  42,  54,  65,  117 
Mesenchyme,  50 
Mesenteries,  dorsal,  f.  54,  f.  55, 152 

formation  of,  150 

ventral,  f.  54,  f.s 5,15 2 
Mesoblast  (=  mesoderm,  q.  v.). 
Mesocardium,  dorsal,  f.  26,  69,  71,  140, 
152 

ventral,  f.  26,  69,  140,  152 
Mesocolon,  153 

Mesocoele    (  =  lumen   of   mesencepha- 
lon, q.  v.). 
Mesoderm,  derivatives  of,  32 

differentiation  of,  37 

dorsal,  f.  17,  f.  29,  f.  54,  38,  47 

early  growth  of,  f.  12,  37 

formation  of,  f.  10,  30 

intermediate,  f.  28,  f.  54,  47,  144 

of  the  head,  40,  50 

regional  divisions  of,  47 

segmental  zone  of,  40 

somatic  layer  of,  f.  28,  f.  54,  49, 
150 

somites  of,  f.  38,  47,  56,  105 

splanchnic  layer  of,  f.  28,  f.  54, 
49,  66,  150,  152 


INDEX 


i6s 


Mesodermic  somites  (see  mesoderm). 
Meso-diencephalic  boundary,  f.  42, 117 
Mesogaster,  153 
Meso-metencephalic  boundary,  f.  42, 

117 
Mesonephric  duct,  f.  51,  f.  52,  f.  53, 

146,  149 
Mesonephric  tubules,  f.  51,  f.  52,  f.  53, 

146,  148 
Mesonephros,  f.  47,  144 
Mesothelium   (=    epithelial  layer  of 

mesoderm  lining  coelom)  f .  54 
Metamerism,  in  mesoderm,  40,  47,  48, 

150 
in  nervous  system,  f .  20,  59 
Metanephros,  f.  51,  144 
Metacoele  (  =  lumen  of  metencephalon 

q.v.) 
Metencephalon,  f.  42,  65,  117 
Metanephric  duct,  f.  51,  146 
Metanephric  tubules,  f.  51,  146 
Mid -brain  (see  mesencephalon). 
Middle  ear,  123 
Mid-gut  (see  gut). 
Morula,  20,  21 
Mouth  opening,  112 
Muscle  plate  (see  myotome). 
Myelencephalic  tela  (=  thin  roof  of 

myelencephalon)   f.   42,    118 
Myelencephalon,  f.  42,  65,  118 
Myeloccele    (=    lumen     of    myelen- 
cephalon q.  v.). 
Myelo-metencephalic  boundary,  f,  42, 

117 
Myocardium,  69,  143 
Myocoele,  107 
Myotome,  f.  38,  f.  44,  107 

Nasal  pit  (see  olfactory  pit). 
Naso-lateral  process,  f.  41,  112 
Naso-medial  process,  f.  41,  112 
Naso-optic  groove,  f.  41 
Neck  of  latebra,  f .  3 
Nephric  tubules,  f.  51,  145 
Nephrostome,  f.  52,  147 
Nephrotomic  plate,  48 
Nerves,  cranial,  118 

spinal,  f.  44,  119 

sympathetic,  t2o 
Neural   cagial     ( =    lumen   of   neural 

tube). 
Neural  crest,  f.  37,  99,  120 


Neural  fold,  f.  17,  42,  45,  99 
Neural  groove,  f.  17, 42, 44 
Neural  plate,  f.  11,  f.  13,  41 
Neural  tube,  52,  99 
Neurenteric  canal,  56 
Neuromeres,  f.  20,  59 
Neuropore,  anterior,  f.  19,  55,  99 

posterior,  56 
Notochord,  f.  11,  f.  13,  40,  55 
Nucleus  of  Pander,  f.  3,  12 

(Esophagus,  f.  43,  loi,  126 
Olfactory  nerve  (=  cranial  nerve  I), 

123 
Olfactory  pit,  f.  40,  f.  41,  f.  46,  112, 123 
Optic  chiasma,  f .  42 
Optic  cup,  f.  42,  95,  121 
Optic  lobes,  117 
Optic    nerve    (=    cranial    nerve    II) 

98,  122 
Optic  stalk,  f.  45,  98,  122 
Optic  vesicle,  primary,  f.  23,  f.  28,  54, 

62,9s 

secondary,  f.  36,  97,  120 
Opticoele  (=  lumen  of  primary  optic 

vesicle,  q.  v.). 
Oral  cavity,  102 
Oral  opening,  1 24 
Oral  plate,  f.  31,  124 
Oral  region,  f,  41,  in 
Orientation  of  embryo  within  egg,  f .  30 
Otocyst  (see  auditory  vesicle). 
Ovum,  fertilization  of.  9 

maturation  of,  9 

ovarian,  f.  i,  7 
Ovulation,  9 

Pancreas,  f.  43,  127 
Pander's  nucleus,  f.  3,  12 
Pellucid  area  (see  area  pellucida). 
Petrosal    ganglion    (=    gangh'on    of 
cranial,  nerve  IX)  f.  42,  118 
Periblast,  10 
Pericardial    region    of    coelom,    f.   24^ 

f.  27,  f.  55,  49,  1^^  150 
Peritoneal  region  of  coelom,  150 
Pharyngeal  pouches,  f.  36,  103 
Pharyngeal  derivatives,  124 
Phar)mx,  f.  35,  loi 
Pigment  layer  of  retina,  f.  45,  96,  122 
Pineal  gland,  95 
Pituitary  body,  95 


z66 


INDEX 


Placodes,  auditory^  65,  122 
lens,  98 

Pleural  region  of  coelom,  f.  46D,  150 

Plica  encephali  ventralis  (=   ventral 
cephalic  fold)  f.  42 

Pocket,  subcaudal,  f.  31,  81 
subcephalic,  f.  31,  47 
Rathke'sf.  35,  f.  43,  95,  117 
Seessell's,  f.  43,  102,  124 

Polar  bodies,  9 

Polyspermy,  10 

Pons,  118 

Post-anal  gut  (see  gut). 

Posterior  appendage  bud,  f.  39,  f.  40, 
112 

Posterior  commissure,  f .  42 

Posterior  intestinal  portal,  f .  3 1 

Posterior  neuropore,  56 

Post-oral  arches,  103 

Post-oral  clefts,  103 

Prechordal  portion  of  brain,  55 

Pre-oral  gut  (see  gut). 

Primitive  groove,  f.  13,  31 

Primitive  gut  (see  gut). 

Primitive    node    (=   Hensen's  node, 
q.  v.). 

Primitive  pit,  f.  13,  28 

Primitive  plate,  f.  29 

Primitive  ridge  or  fold,  f.  13,  28 

Primitive  streak,   as   growth   center. 

33 
fate  of,  56 

formation  of,  f.  9,  f.  10,  28 
interpretation  of,  f.  9,  f.  10,  28, 

35 
location  of,  f.  8,  f.  11,  27 

Primordial    follicle    ( =    very    young 
ovarian  follicle)  f.  i 

Proamnion,  f.  12,  37 

Proctodaeum,  f.  31,  130 

Pronephros,  f.  51,  144 

Pronephric  duct,  146 

Pronephric    tubules   of  chick,  f.    52, 
146 

Prosencephalon,  f.  20,  54,  61,  95,  114 

Prosocoele     (=      lumen    of     prosen- 
cephalon, q.  v.). 

Ramus  communicans,  119 
Rathke's  pocket,  f.  35,  f-  43>  9S»  ii7 
Recapitulation,  43,  102,  144 
Recessus  neuroporicus,  f.  42 


Recessus  opticus,  f.  42,  115 
Reduction  division  of  gametes,  9 
Retina,  pigment  layer  of,  f.  45,  96, 122 
sensory  layer  of,  f.  45,  96,  122 
Rhombencephalon,  f.  20,  54,  61,  65 
Rhombocoele  (=  lumen  of  Rhomben- 
cephalon, q.  v.). 
Roof  plate  of  spinal  cord,  119 

Sclera  of  eye,  122 

Sclerotomes,  f.  38,  f.  44,  107 

Sections,  location  of,  4,  34 

Seessell's  pocket,  f.  43,  102,  124 

Segmentation,  14  (see  also  cleavage). 

Segmentation  cavity  (see  blastocoele). 

Sensory  layer  of  retina  (see  retina). 

Septa  of  yolk  sac,  f.  30,  84 

Serial  sections,  4 

Sero-amniotic  cavity,  f.  30,  f.  32,  87 

Sero-amniotic  raphe,  f.  30,  f.  32,  87 

Serosa,  f.  30,  f.  32,  86 

Sex  cells  (see  gametes) . 

Shell,  f.  3,  10 

Shell  membranes,  f.  3,  10 

Sinus  region  of  the  heart  (see  sinus 

venosus). 
Sinus  rhomboidalis,  f.  21,  55,  99 
Sinus    terminalis   (=    terminal    vein, 

q.  v.). 
Sinus  venosus,  f.  23,  f.  49,  f.  50,  72 
Somatic  mesoderm  (see  mesoderm). 
Somatopleure,  f.  17,  49 
Somites,  diflferentiation  of,  f.  38,  105 

formation  of,  56 
Spermatozoa,  f.  2,  10 
Spinal  cord,  54,  118 
Spinal  ganglia  (see  ganglia). 
Spinal  nerve  roots,  development  of, 

f.  44,  IT9 

Splanchnic  mesoderm  (see  mesoderm). 
Splanchnopleure,  f.  17,  49 
Stomach,  f.  43,  126 
Stomodaeum,  f.  31,  f.  35,  loi,  124 
Subcaudal  space  or  pocket,  f.  31,  81 
Subcephalic  space  or  pocket,  f.   17, 

f.  31,  47 
Subgerminal    cavity    (=     blastoccele 

q.  v.). 
Sylvian  aqueduct,  f.  42,  117 
Sympathetic  ganglia,  f.  44,  j2o 
Sympathetic  nerve  roots  (see  ramus 

communicans). 


INDEX 


167 


Tail,!.  39, 81 

Tail  fold  of  amnion,  f.  32,  87 

Telencephalon,  later  development  of, 

"5 

lateral  vesicles  of,  f.  42,  114 

median,  f.  42,  114 

origin  of,  65,  95 
Teloccele  (=  lumen  of  telencephalon, 

q.  v.). 
Telo-diencephalic  boundary,  115 
Telolecithal  ova,  f.  4,  15 
Thalami  (optici),  117 
Theca  folliculi,  f.  i,  8 
Thymus,  125 

Thyro-glossal  duct,  f.  43,  125 
Thyroid  gland,  125 
Torsion  of  embryo,  f.  29,  75,  109 
Trabeculae  carneae,  f,  46D,  144 
Trachea,  f.  43,  125 

Trigeminal    ganglion    (=     Gasserian 
ganglion    of    cranial    nerve 
V,q.v.). 
Trigeminal  nerve  (=    Cranial  nerve 

V),  118 
Tuberculum  posterious,  f.  42, 117 

Ureter    (derived    from    metanephric 
duct,  q.  v.). 

Vagus  nerve  (=«  cranial  nerve  X),  118 

Vegetative  pole,  8 

Vein,  allantoic,  f.  47 

cardinal,  ant.  f.  24,  74,  105,  139 

cardinal,  common    (=    Duct    of 

Cuvier)  f.  24,  f.  47,  74,  105 

cardinal,  posterior,  f.  24,  74,  105, 

139 
definition  of,  133 
omphalomesenteric,  f.  21,  f.  47, 

57,  74,  105,  127 
terminal    (=    sinus    terminalis), 

f.  21,  f.  48,  136 


vena  cava,  139 
vitelline,  f.  48 
Velum  transversum,  f.  42,  115 
Ventrad,  usage  of  term,  5 
Ventral,  usage  of  term,  5 
Ventral  aorta  (see  aorta). 
Ventral  aortic  roots  (see  aortic  roots) . 
Ventral  cephalic  fold,  f .  42 
Ventral  ligament  of  liver,  153 
Ventral  mesentery  (see  mesenteries). 
Ventral     mesocardium     (see     meso- 

cardium). 
Ventral  nerve  roots,  f.  44,  119 
Ventricle,  f.  23,  f .  49,  f.  50,  72,  141 
Ventro-lateral   pancreatic   buds,    127 
Visceral  arches,  f.  34,  f.  40,  f.  46,  102, 

III 
Visceral  clefts,  f.  34,  f.  40,  102,  11 1 
Visceral  furrows,  f.  36,  f.  46,  103 
Visceral     pouches      (=      pharyngeal 

pouches),f.36, 103, 125 
Vitelline  blood-vessels  (see  arteries  and 

veins) . 
Vitelline  circulation  (see  circulation). 
Vitelline  membrane,  f.  i,  f.  3,  8. 
Vitreous  body  of  eye,  122 

Wolffian  body  ( =mesonephros,  q.  v.). 
Wolffian  duct   (=  mesonephric  duct, 
q.  v.). 

Yolk,  absorption  of,  84,  136 

effect  of  on  gastrulation,  f.  6,  21 

effect  of  on  segmentation,  f.  4,  14 

white,  f.  I,  f.  3,  12 

yellow,  f.  I,  f.  3,  12 
Yolk  duct,  84 

Yolk-sac,  f.  30,  f.  32,  81,  84,86 
Yolk  stalk,  f.  30,  f.  31,  f.  32,  84 

Zona  radiata,  f.  i,  8 

Zone  of  junction,  f.  7,  21,  24 

Zones  of  the  blastoderm,  24 


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25w-10.'67(H552584)4128 


413^1 


